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Effects of Ultrasound Modes on Mandibular Osteodistraction
T.H. El-Bialy1,*,
R.F. Elgazzar2,
E.E. Megahed3 and
T.J. Royston4
1 Orthodontics and Biomedical Engineering, Faculty of Medicine and Dentistry, University of Alberta, Dentistry/ Pharmacy Centre, Room 4051, Edmonton, AB, Canada T6G 2N8, formerly Lecturer of Orthodontics, Tanta University, Egypt;
2 Oral and Maxillofacial Surgery/Dental Diagnostic and Surgical Sciences, Faculty of Dentistry, University of Manitoba, Canada, and Faculty of Dentistry, Tanta University, Egypt;
3 Oral Pathology, Tanta University, Egypt; and
4 Mechanical Engineering, University of Illinois at Chicago, USA
Correspondence: * corresponding author, telbialy{at}ualberta.ca
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ABSTRACT
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Previous studies have shown that therapeutic pulsed ultrasound (pulsed) has superior stimulatory effect on bone fracture healing compared with continuous ultrasound (continuous). Our predictive hypothesis was that pulsed ultrasound can produce better bone formation during mandibular osteodistraction than continuous ultrasound. Thirty-six New Zealand rabbits were divided into 3 groups of 12. Osteodistraction was performed at 3 mm/day for 5 days. Group 1 received pulsed, group 2 received continuous ultrasound, and group 3 was the control group (distraction only). Bone formation was assessed by quantitative bone density (QBD), mechanical testing, and histological examination. In the first 2 wks post-distraction, group 2 showed enhanced bone formation more than group 1 (p < 0.05); however, in the 3rd and 4th wks, group 1 showed more bone formation than group 2 (p < 0.05). Earlier stages of bone healing were enhanced more by continuous, whereas late stages were enhanced more by pulsed, ultrasound. Abbreviations: PULSED, low-intensity pulsed ultrasound; CONTINUOUS, low-intensity continuous ultrasound.
Key Words: mandibular bone healing • bone formation • distraction osteogenesis • therapeutic ultrasound
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INTRODUCTION
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Distraction osteogenesis is considered a successful technique to gain bone and soft-tissue mass in persons with a variety of craniofacial deformities (McCarthy et al., 1992; Molina and Ortiz Monasterio, 1995; Dessner et al., 1999; Sadakah et al., 2006). However, mandibular osteodistraction may be affected by masticatory muscle forces that may lead to bending of the newly formed bony callus (Dessner et al., 1999). To overcome this problem, many studies have evaluated different techniques to enhance bone healing during osteodistraction (e.g., insulin-like growth factor (Stewart et al., 1999) and electrical stimulation (Hagiwara and Bell, 2000).
Pulsed ultrasound has been used to enhance bone fracture healing (e.g., Pilla et al., 1990; Heckman et al., 1994; Kristiansen et al., 1997). Ultrasound at 0.5 W/cm2 was found to be stimulatory to fracture repair, if given for 15 min/day. However, ultrasound at the intensity of 1.0 W/cm2 was found to be deleterious to the treated fracture (Tsai et al., 1992). Pulsed ultrasound (30 mW/cm2) was reported to enhance healing after osteodistraction of the tibia in a rabbit model (Shimazaki et al., 2000), after metatarsus osteodistraction in sheep (Mayr et al., 2001), and after mandibular osteodistraction in rabbits (Hagiwara and Bell, 2000; El-Bialy et al., 2002; Tis et al., 2002), and this effect is dose-dependent (Chan et al., 2006). It has been reported that pulsed ultrasound does not induce bone formation during tibial osteodistraction (Taylor et al., 2007). This, however, could be due to the fact that these investigators used a slow rhythm and rate of distraction of 0.5 mm/12 hrs. In addition, it was reported that pulsed ultrasound enhances bone formation after osteodistraction in humans (El-Mowafi and Mohsen, 2005; Schortinghuis et al., 2005).
Pulsed and continuous ultrasound modes have been tested for enhancing endochondral ossification in vitro (Wiltink et al., 1995). Pulsed ultrasound resulted in significantly increased longitudinal growth after 4 days, while continuous ultrasound showed growth after 16 days. The exact effect of pulsed ultrasound is not clearly understood. It could be due to the effect of pulsation or the thermal effect of the low level of power output. The aim of this study was to evaluate the effect of pulsed and continuous ultrasound on bone healing during mandibular osteodistraction in rabbits.
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MATERIALS & METHODS
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Thirty-six New Zealand, skeletally mature, male rabbits, each weighing from 3 to 3.6 kg, were used in this study and were divided into 3 groups of 12 each according to the treatment received (pulsed, continuous ultrasound, or control [distraction only]). According to the endpoint (1, 2, 3, or 4 wks), each group was subdivided into 4 subgroups of 3 animals each. The experimental protocol was approved by the Animal Care Committee at the University of Illinois at Chicago (No. 1999-076). All animals were operated on while under general anesthesia induced by an intramuscular injection of 50 mg/kg ketamine aided by 5 mg/ kg xylazine. The skin over the operative area was prepared, then both sides of the mandible were exposed through a submandibular incision. An osteotomy was made on the buccal side through the anterior part of the mandible, just anterior to the first molar, with the use of a tapered fissure bur cooled with water. Four holes were drilled, 2 on each side of the corticotomy, and a custom-made osteodistractor (Oral Osteodistraction Ltd., Buffalo Grove, IL, USA) was applied and positioned under the inferior border of the mandible. We activated it 72 hrs after surgery by opening the screws 1.5 mm every 12 hrs for 5 days. During surgery, a 5–8 Nasoesophageal tube was inserted and sutured to the rabbit’s face for post-operative feeding. Prophylactic antibiotics and painkillers were injected subcutaneously for a few days. Pulsed ultrasound was applied by means of a SAFH system (Exogen Inc., Piscataway, NJ, USA), and the ultrasound output was 200-µs pulses of 1.5 MHz at a 1.12-KHz pulsing frequency (duty cycle of 22:4%) for 20 min every day. Continuous ultrasound was applied with the same SAFH transducer, while the circuit was modified to produce continuous modes of the same frequency (1.5 MHz) and output power (30 mW/ cm2) (Figs. 1A, 1B ).
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Figure 1. Histological examination for all groups at the end of each week (hematoxylin & eosin x 100). Scale = 100 µm. (A) Ultrasound device used. (B) Pulsed ultrasound during application to the rabbits’ mandibles. (C) (PULSED W1) Photomicrograph of PULSED 1 wk after distraction, revealing the junction between the old bone and the newly formed bone. Osteoblasts are clearly seen in the bone marrow rimming the bone trabeculae. (D) (CONTINUOUS W1) Photomicrograph of CONTINUOUS 1 wk after distraction, showing that the bone trabeculae is bigger than in the other groups. Osteoblasts are clearly evident rimming the bone trabeculae in the PULSED group, but are not detected in the CONTINUOUS group. (E) (CONTROL W1) Photomicrograph of the distraction group 1 wk after distraction, showing weak junction between the old bone and the newly formed bone. (F) (PULSED W2) Photomicrograph of PULSED at week 2, showing a greater number of bone trabeculae than in the other groups, and also abundant numbers of osteoblast cells rimming the bone trabeculae, while osteoblast cells were not evident in the other groups. (G) (CONTINUOUS W2) Photomicrograph of CONTINUOUS at week 2 showing the newly formed bone undergoing remodeling, ranging from woven at the center of the distracted area to well-organized lamellar bone at the periphery of the distracted area. The bone marrow is filled by fat cells. (H) (CONTROL W2) Photomicrograph of the distraction group, 2 wks after distraction, showing less ossification than in the other groups. (I) (PULSED W3) Photomicrograph of PULSED, at week 3, demonstrating newly formed bone trabeculae rimmed by osteoblast cells. (J) (CONTINUOUS W3) Photomicrograph of CONTINUOUS at week 3, demonstrating the center of the distraction zone filled with fibrous tissue. (K) (CONTROL W3) Photomicrograph of the distraction group at week 3, showing the junction of the newly formed bone trabeculae with the old bone. (L) (PULSED W4) Photomicrograph of PULSED at 4 wks, showing the great amount of immature bone trabeculae at the distracted zone and bone trabeculae rimmed by osteoblast cells. The bone marrow is delicate in nature and highly vascular. (M) (CONTINUOUS W4) Photomicrograph of CONTINUOUS at 4 wks, showing the center of the distraction zone filled by a dense bundle of collagen fibers (Masson’s trichrome x 40). (N) (CONTROL W4) Photomicrograph of the distraction group at 4 wks.
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Ultrasound treatments were applied to both sides of the mandible. Since previous studies (Tsai et al., 1992; Guerrissi et al., 1994; Stewart et al., 1999) found that the major significant differences in bone formation occurred during the first 3–4 wks, animals in this study were killed at 1, 2, 3, and 4 wks after the conclusion of distraction, by an IV overdose of sodium thiopental. The mandible was dissected and split in half. Halves of the mandibles of each group were preserved in buffered saline at 4°C for mechanical testing/bone mineral density (QBD), with a CT scan and bone phantom studies. The other halves were fixed in 10% buffered formalin, and then decalcified with EDTA and stained by hematoxylin and eosin and Masson’s trichrome for histomorphometric studies.
Quantitative Bone Density with Computed Tomography and Bone Phantom
We used an Imatron C150 computerized tomography machine (Rush University Medical Center, Chicago, IL, USA) to obtain images of the rabbit mandibles with a resolution of 512 x 512 pixels for a 9-cm-diameter scan window with 0.5-mm axial increments normal to the slice plane. A phantom with 5 regions within a gel pack was used for QBD. For bone mineral density (BMD) calculations, we used Accuview software (NVIDIA Corp., Santa Clara, CA, USA) to export the images as bitmaps, and then transform the images to 8-bit, 256-grayscale levels. Adobe Photoshop software was then used to determine BMD within the mandible via interpolation (quantitative comparison) of the grayscale level as compared with the 5 phantom markers. These phantom regions contain: (1) a fat-mimicking polymer, (2) water, (3) 50, (4) 100, and (5) 200 K2HPO4 in water. BMD values in g/cm2 for bone at the distraction region were calculated as a percentage of that of the original cortical bone adjacent to the distraction site. The technique has been described in the literature (Chalmers et al., 2006; Tzaphlidou et al., 2006; Hangartner and Short, 2007; Schweizer et al., 2007).
Mechanical Testing
A three-point bending mechanical test was performed with an Instron No. 5500 servohydraulic materials testing machine (Instron, Canton, MA, USA) at all distraction sites for all groups. The samples were tested in a simply supported configuration and loaded on the lateral aspects of the mandibles. The displacement rate was 1 mm/sec. The stiffness of the half-mandibular structure was calculated as the slope of the initial linear segment on the load deflection curve in N/mm.
Histological Examination and Histomorphometric Analysis
Histological examination was studied qualitatively and quantitatively by histomorphometric techniques. The analysis of new bone was performed in regions with, subjectively, the highest number of bone trabeculae. Four adjacent medium-power microscopic fields (100 µm2) were analyzed. Bone trabeculae were automatically counted in the selected microscopic fields with the use of image analysis software (Image J, 1.29z, NIH, Bethesda, MD, USA). Images were automatically corrected for brightness and contrast, then were converted into 8-bit grayscale, and an automated counting of bone trabeculae was performed. The average size of bone trabeculae, total area, and area fraction were also measured. Bone volume/tissue volume was used for bone histomorphometric analysis in all groups (Fink et al., 2003).
Statistical analysis was performed with the Minitab 13.1 Statistical Package. Descriptive statistics included mean and standard deviations as well as a one-way analysis of variance test to compare QBD, bone stiffness, as well as bone volume/tissue volume histomorphometric analysis at the distraction sites between the groups. The level of significance was set to 95%.
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RESULTS
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All animals survived the operation and follow-up period. Wound healing was noticed in all animals; there were no signs of infection, dehiscence, or other pathology.
Quantitative Bone Density
Comparisons of BMD values for the newly formed bone at the distraction site, normalized to the neighboring normal bone by use of the BMD of the neighboring bone as a self-reference in all groups, are presented (Table, Fig. 2A). In the first 2 wks after the completion of distraction, better bone density was produced by continuous compared with pulsed ultrasound; however, in the 3rd and 4th wks, pulsed produced better bone density than continuous ultrasound (p <0.05).
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Figure 2. Graphic representation of comparison of different variables between and among groups. N = 3 in each subgroup. (A) The mean and standard deviation of the QBD normalized (percentage of the QBD of the distraction site to that of normal bone) for all groups over the four-week period. (B) Mean ± standard deviation of the mechanical stiffness for all groups over the four-week period. (C) The mean ± standard deviation of the percentage of the bone volume/tissue volume % (BV/ TV) representing the amount of bone formation for all groups over the four-week period.
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Mechanical Stiffness Test
Comparisons between the stiffness of the distraction site in all groups at the end of each week of the 4 post-operative wks are presented (Table , Fig. 2C). It can be seen that the distracted bone treated with pulsed ultrasound had a higher stiffness compared with that treated with continuous ultrasound and compared with the control group (pulsed > continuous > control group).
Histological Evaluation and Bone Histomorphometric Analysis
At 1 wk after the completion of distraction, fibrous connective tissue was evident in the distraction gap. Collagen fibers were stretched out and oriented to the direction of distraction, and slightly immature bone was visible at the distraction edges. However, newly formed bone in the stimulation groups was obviously greater than in the control group. The size of the bone trabeculae was bigger in the continuous group than in the other groups, and the bone trabeculae in the distraction group were thin and long. Osteoblasts were clearly evident, rimming the bone trabeculae in the pulsed group, while this was not detected in the continuous group. As well, there were abundant small blood vessels and a few islands of cartilage in both ultrasound groups (Figs. 1C, 1D, 1E).
At 2 wks, in all groups, regenerated bone was seen along the collagen fibers except for a small gap in the center of a distracted segment filled by fibrous tissue. The pulsed group contained the highest number of bone trabeculae when compared with the other groups; this group also contained abundant numbers of osteoblasts rimming the bone trabeculae, whereas osteoblast cells were not evident in the other groups. The newly formed bone was undergoing remodeling ranging from woven at the center of the distracted area to well-organized lamellar bone at the periphery of the distracted area. Bone marrow in the continuous group was filled with fat cells (Figs. 1F, 1G, 1H).
After 3 wks of stabilization, there were fewer bone trabeculae in the continuous group than in the pulsed group, and they appeared to be lamellar (Figs. 1I, 1J, 1K). At week 4, the regenerated new bone completely filled the distraction gap in the pulsed group with a thickened network of immature woven bone (Figs. 1L, 1M, 1N). This group was also characterized by a predominance of osteoblast cells and with delicate and highly vascular marrow spaces. In the continuous group, there was a deficiency in bone formation in the center of the distraction zone, which still contained fibrous tissue. Bone trabeculae appeared to be small and lamellar. Osteoblast cells were not evident, and the marrow spaces were fibrotic. Bundles of collagen fibers were clearly evident in this group. In the control group, there were fewer bone trabeculae, and they were small. The distraction gap had fibrous tissue in the center.
In general and at the end of the 4 wks of study, the bone volume/tissue volume % was found to be higher in the ultrasound (pulsed or continuous) treated groups compared with the non-treated group (p < 0.05). Also, the results showed that the pulsed group had higher bone volume/tissue volume % compared with the continuous treated group. There were no statistically significant differences between the two groups at the first 2 wks. However, the differences were statistically significant at the 3rd and 4th wks in terms of the percentage of the bone trabeculae and the total bony areas (Fig. 2B, Table).
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DISCUSSION
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The increased number of cartilage foci in the control group could be due to low oxygen tension in the tissue. In contrast, increased vascularity in the experimental group (continuous or pulsed) could be due to the stimulatory effect of ultrasound on angiogenesis, with subsequent high oxygen tension that enhanced intramembranous bone formation (Ilizarov, 1989; Karaharju-Suvanto, 1992; Peltonen et al., 1992). In our study, the ultrasound-treated groups had higher amounts of regenerated bone in comparison with the control group. The effect of ultrasound on regenerated tissue and bone has been reported in several studies (Dyson et al., 1968; Harris, 1992; Wang et al., 1994; Yang and Park, 2001); all results of these studies confirmed the positive effect of ultrasound on the stimulation of osteoblasts and fibroblasts, proliferation, and enhancement of healing and bone formation. But to what extent are the modes of ultrasound applications effective? In the present study, continuous had nearly the same effect as pulsed ultrasound in the first 2 wks of application; but during the last 2 wks of application, the effect of continuous ultrasound began to regress. In the continuous group, the regenerated bone trabeculae appeared lamellar, even in week 4 at the center of the distraction zone, which was not filled by bone, but still had dense bundles of collagen fibers, while the regenerated bone in the pulsed group was completely filled by woven bone. This may be explained, since the pulses of the pulsed mode could be providing additional mechanical stimulation that had a stimulatory effect on bone cell differentiation and bone matrix production. Physiological strain stimulated osteoblastic differentiation and early mineral deposition, whereas higher strain magnitudes led to the formation of fibroblast-like cells surrounded by collagen fibrils and only slight mineralization (Meyer et al., 1999). It has been reported that one of the cellular mechanisms underlying the therapeutic action of ultrasound is mechanical. The ultrasound pressure wave deforms connective tissue cell membranes, altering their ionic permeability, and so activates the intracellular second-messenger adenylate cyclase (Hadjiargyrou et al., 1998). Also, it has been reported that ultrasound stimulates the production of vascular endothelial growth factor, which is an important factor in new blood vessel formation (angiogenesis), which in turn is an important factor in bone formation (Reher et al., 1999). In contrast, continuous ultrasound, when applied for pre-determined time intervals, possessed higher cellular viability (1.2 to 1.4 times) and higher levels of type II collagen and aggrecan mRNA expression in chondrocytes when compared with controls (Noriega et al., 2007). It is obvious that either the pulsation of the pulsed or the intermittent application of the continuous ultrasound is important in stimulation of bone formation and cellular responses. We can conclude that bone formation by rapid distraction osteogenesis (3 mm/day) of the mandibular bone can be improved with both pulsed and continuous ultrasound. Sensitivity of the regenerating bone to ultrasound stimulation is stage-dependent. Earlier stages of bone healing were enhanced more by continuous, whereas late stages were enhanced by pulsed, ultrasound.
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ACKNOWLEDGMENTS
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Funding for this research was provided by the University of Illinois at Chicago (UIC), Campus Research Board. The authors thank Akira Sakata, Department of Mechanical Engineering, and Dr. James Drummond, Biomaterials, Faculty of Dentistry, UIC, for their help with the mechanical testing. Also, the authors thank Oral Osteodistraction Ltd. (Buffalo Grove, IL, USA), for their donation of the distraction devices. Also, we thank Exogen, Inc. (Piscataway, NJ, USA) for providing the pulsed ultrasound device.
Received for publication August 9, 2007.
Revision received May 22, 2008.
Accepted for publication June 9, 2008.
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Journal of Dental Research, Vol. 87, No. 10,
953-957 (2008)
DOI: 10.1177/154405910808701018
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[Abstract]
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ABSTRACT
INTRODUCTION