PHYS THER
Vol. 79, No. 10, October 1999, pp. 931-938
Can Some Physical Therapy and Manual Techniques Generate Potentially Osteogenic Levels of Strain Within Mammalian Bone?
Andrew W Wilson,
Helen MS Davies,
Glenn A Edwards and
Brian L Grills
AW Wilson, MManipTherapy, DipPhysPT, is a part-time PhD student, School of Human Biosciences, Faculty of Health Science, La Trobe University, Melbourne, Victoria, Australia. Address all correspondence to Mr Wilson at School of Human Biosciences, Faculty of Health Sciences, La Trobe University, Bundoora, Victoria, Australia 3083 (a.wilson{at}latrobe.edu.au)
HM Davies, PhD, is Lecturer in Anatomy, Department of Veterinary Science, University of Melbourne, Parkville, Victoria, Australia
GA Edwards, BVSc, is Senior Lecturer in Small Animal Surgery, Department of Veterinary Science, Veterinary Clinic and Hospital, Princes Highway, Werribee, Victoria, Australia
BL Grills, PhD, is Lecturer in Pathophysiology, School of Human Biosciences, Faculty of Health Sciences, La Trobe University, Bundoora, Victoria, Australia
Submitted August 23, 1998;
Accepted June 30, 1999
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Abstract
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Background and Purpose. Although physical therapy techniques are used to alleviate pain and stiffness in joint injuries, whether these methods are capable of affecting bone is unknown. For example, can these techniques potentially influence bone formation or resorption? To begin exploring this possibility, this study investigated the ability of 4 manual techniques to generate levels of compressive strains that presumably can stimulate bone metabolism. Subjects. Six 3,4 metacarpals from three 3-year-old Merino ewes were used. Methods. A rosette strain gauge was implanted onto the dorsomedial cortex of each ovine 3,4 metacarpal. Four different manual procedures were applied on 2 occasions on each metacarpal in vivo and ex vivo. Mean peak principal compressive strains were calculated for each technique. Results. Levered bending produced greater mean peak compressive strains than almost all other manual procedures tested in vivo or ex vivo. Conclusion and Discussion. Manual levered bending created levels of compressive strain similar in magnitude to those created by mechanical devices used in previous animal experiments to induce new bone formation (osteogenesis). This animal model appears to be suitable for investigating the effects of manually applied procedures on bone and may establish whether manual techniques can stimulate bone formation.
Key Words: Compressive strain • Manual techniques • Mechanical forces • Metacarpal bone • Osteogenesis
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Introduction
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Physical therapists use manually applied techniques in the treatment of injuries to the musculoskeletal system. Manual techniques have been utilized in the treatment of arthritic joints, but these procedures have been performed largely to decrease joint pain and stiffness,1 rather than to encourage bone healing. To our knowledge, there has been no controlled study that has attempted to influence bone formation or bone resorption.
Bone is extremely sensitive to the mechanical forces to which it is exposed.2 Change in the internal architecture or the size of bone can occur in response to the mechanical loading to which bone is subjected.3 This process was first described in Wolff's law,4 which proposes that the form and function of bone is produced by alterations in its internal architecture that occur according to "self-ordered" mathematical rules. A morphological change in bone, therefore, can result from a change in loading. For example, an increase in the functional demands made of a skeleton will result in site-specific increases in bone mass; conversely, a decrease in functional use leads to site-specific bone resorption, and maintenance of functional loading helps to maintain bone mass.3,5 This process allows the skeleton to adapt optimally to functional load bearing without being burdened by the weight of any unnecessary bone. Research over the past 30 years has attempted to discover what triggers the process of functional adaptation in accordance with Wolff's law.
The magnitude, orientation, and distribution of strains encountered by bone during functional activities are deemed to be extremely important in controlling bone mass.6–13 The biomechanical term "strain" is defined as 
l/L, where l=the change in length and L=the original length. Negative strain values refer to compressive loading, whereas positive strain values refer to tensile loading.14 It has been determined that osteogenesis can result from the application of physiological levels of compressive bone strain even if applied in a manner that bone would not encounter during life.15,16 Physiological activities, such as running, create similar levels of bone strain across different species, regardless of species size, that approaches –3,000 microstrain (µstrain) in magnitude as a maximum.17 Lanyon and Rubin18 determined that dynamic compressive loads applied intermittently were more effective than constant compressive loads in stimulating osteogenesis in avian bone. Further work by Rubin and Lanyon19 involving stimulation of intact turkey bone utilizing a mechanical device demonstrated a linear dose-response relationship between peak strain magnitude greater than –1,000 µstrain and the area of osteogenesis that was stimulated. The number of cycles required to produce this response was as small as 36 consecutive load cycles. All of these experiments used a loading frequency of 0.5 Hz.
Manual physical therapy techniques can apply dynamic compressive forces at a frequency of 0.5 Hz.20 If manual procedures are able to create compressive strains in excess of –1,000 µstrain with an abnormal strain distribution within a bone, they could potentially stimulate osteogenesis in that bone. An animal model, therefore, could be devised in which the effect of manually applied treatment techniques can be determined. Such an animal model could help to describe the effect of manually applied mechanical force on intact bone and bone cells in vivo. This knowledge may indicate whether there is any role for manual physical therapy techniques in the treatment of people with bone disorders. The purpose of our study was to quantify the magnitude of compressive strains that 4 different manual procedures could create within the ovine 3,4 metacarpal in vivo and ex vivo.
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Method
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Subjects
Three 3-year-old adult Merino ewes were used for this study. Animals 1 and 3 weighed 55 kg, and animal 2 weighed 65 kg. All animals were bred from the same flock of sheep. The ovine 3,4 metacarpal bone is approximately 12 to 13 cm in length. This bone, in our opinion, was large enough (approximately 2 cm in diameter) to allow the application of manual techniques, and it had the advantage of having few muscular origins or insertions, except the insertion of the extensor carpi radialis muscle into the dorsomedial surface of the proximal end of the bone. Any muscular contraction in the limb of the animal did not produce any loading of the bone underneath a strain gauge. The site selected for the application of the strain gauge on the 6 metacarpals was on the dorsomedial surface approximately 60% of the distance between the proximal and distal ends of the metacarpal bone.
Strain Gauge Assembly and Implantation
Stacked rectangular rosette strain gauges (series WA-09-060-WR-120)* were used on both left and right metacarpals of all 3 animals. The gauges were prepared following a technique that has been described elsewhere.21 The animals were anesthetized with an intravenous injection of thiopentone and were maintained under anesthesia by intubation and delivery of oxygen and halothane. The anterior surface of each metacarpal was clipped, and an Esmarch bandage was applied to restrict blood flow to the distal limb and metacarpus. A 6-cm vertical incision was made over the dorsum of the 3,4 metacarpal, the soft tissues were retracted, an area of periosteum measuring 12 x 12 mm was removed, and the bone was scraped clean. The bone surface was swabbed with absolute alcohol, allowed to dry, and then covered with a thin layer of adhesive (isobutyl-2-cyanoacrylate [Histoacryl])
to seal any areas of potential hemorrhaging. Another layer of adhesive was placed over the gauge backing and implantation site. The gauge was then positioned quickly and held in position with thumb pressure over a Teflon
film for 2 minutes.
The lead wires from the strain gauge were passed through a stab incision 4 to 5 medial and proximal to the original incision and then sutured and glued to the skin, leaving a large loop of wire between the bone and skin exit. The position of each gauge was marked with a skin tattoo
measuring 1.5 x 1.5 cm placed on the skin overlying the gauge site.
An intramuscular injection of penicillin-streptomycin (Ilium)|| was given to each animal following wound closure to prevent infection. None of the animals were lame after surgery.
Manual Stimulation
In vivo.
The techniques of 4-point bending, shear bending, levered bending, and torsion-rotation were used to load the area of bone underneath the strain gauge both in vivo and ex vivo. These techniques are illustrated in Figures 1
through 4. The 4 different manual techniques were selected to represent different methods of producing compression. The manual techniques were performed in vivo the day after surgery and then repeated 2 days later. None of the animals appeared to be distressed by the performance of the manual techniques. Prior to in vivo testing, the gauges were tested for patency. Five of the 6 gauges were intact. Two out of 3 elements of the gauge on the right metacarpal of animal 2 were functioning properly, and it was not possible to determine the exact maximum and minimum principal strains that occurred during manual stimulation in vivo in this bone. Data from this metacarpal were not included for analysis. All techniques were performed for 30 consecutive load cycles. A rest period of 1 minute was allowed between techniques. Each technique was performed twice on each metacarpal at each of the 2 testing sessions.
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Figure 1. Four-point bending. Arrows indicate direction of applied force. "G" indicates gauge position.
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All techniques were performed in the in vivo phase of the experiment with the sheep immobilized in dorsal recumbency on a surgical frame. All uninvolved limbs were immobilized in stirrup straps, and the remaining metacarpal was free to receive manual stimulation. A small block of wood measuring 11.5 x 4.5 x 1 cm was placed underneath the dorsal surface of the metacarpal proximal to the strain gauge to help improve fixation. Care was taken with both the wooden block and the manipulator's hands to ensure that placement of the block and hands was close to, but not directly over, the implantation site. The gauges were connected to signal-conditioning amplifiers (model 2120A)# and were checked and calibrated at the beginning of each application of each manual technique. Strain gauge data were recorded into a computer (MacSE-30) via a MacLab A/D converter** at a sampling rate of 40 Hz per channel.
The peak principal strain during each manual maneuver was determined by combining the data from the 3 gauges in each rosette using the principles of Mohr circle analysis.22 Deformation of any solid such as bone creates deformation simultaneously in vertical, horizontal, and transverse directions in differing proportions depending on the force used. The principal strain is the resultant strain measured by the 3 different gauge elements of each rosette, with each element aligned in a different direction.23 Mean peak compressive strains were determined for 6 cycles of each manual technique application by selecting 6 cycles of manual loading with the greatest magnitude of compressive strain. All selected strain gauge data were analyzed by Rosette for Windows computer software* to calculate the maximal tensile and compressive principal strains and the strain rate. The peak compressive strain for all manual procedures was recorded by selecting the load cycle that engendered the greatest compressive strain within the bone surface underneath the strain gauge.
The strain rate measures the rate of change in strain magnitude over time.17 The mean peak strain rate was calculated by combining the peak strain rate from 6 cycles of maximal compressive peak strain occurring during a single technique application and combining them to determine a mean value for each technique on each metacarpal.
Ex vivo.
At the end of the in vivo test period, all sheep were killed by an intravenous overdose injection of sodium pentobarbitone (Lethabarb),** and all 6 metacarpal bones were harvested with the phalanges, hoof, soft tissues, and gauges intact. The metacarpals were labeled and then stored deep frozen to –20°C. The ex vivo testing phase began several weeks after the sheep were sacrificed. All metacarpals were thawed for at least 24 hours prior to ex vivo testing. Prior to loading, the skin incision was reopened, and gauge position and adherence to the bone surface were confirmed in all metacarpals. Circuit patency was tested. Four of the 6 metacarpals had functioning circuits. The remaining 2 gauges were nonfunctional and were not used for ex vivo testing. Each manual procedure was performed for 30 load cycles on each metacarpal twice on 2 different testing days. The ex vivo metacarpal was placed over the edge of a wooden table, and the position of the gauge was confirmed by visual identification of the gauge on the bone surface and its position relative to the edge of the table. Visual positioning of the gauge ensured that deformation of the gauge did not occur by direct contact of the operator's hands or the wooden table. The data were recorded into a computer in the manner described for in vivo loading.
Data Analysis
Two-way analyses of variance (ANOVAs) were performed on the data from the in vivo (df=4, n=5) and ex vivo (df=3, n=4) manual procedures. The data were collapsed to provide a mean for each technique on to each bone and a mean for each technique on all bones to allow post hoc testing using a t test for comparison between means. A paired t test was done for each manual technique when performed in vivo and ex vivo to determine whether there were any differences in the level of compressive strain engendered within a technique when performed in vivo and ex vivo. Results were considered significant at P<.05.
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Results
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In Vivo Testing
The mean peak strain magnitude of each technique application in vivo is presented in Table 1. A 2-way ANOVA revealed a difference in the magnitude of strain created between the manual procedures used in this study (P <.001). Post hoc testing using a t test revealed differences between means of the different techniques. Both levered bending (–1,308 µstrain) and shear bending (–926 µstrain) created higher compressive strains than those created by 4-point bending (–575 µstrain) and torsion-rotation (–353 µstrain) (P <.001), but no difference was apparent when levered bending (–1,308 µstrain) and shear bending (–926 µstrain) were compared with each other. Four-point bending (–575 µstrain) was able to engender higher compressive strains than torsion-rotation (P <.01). The highest mean peak compressive strain produced by the application of manual techniques was –1,660 µstrain, which was created by the application of levered bending to metacarpal 4. The greatest peak compressive strain produced by any of the manual procedures was –2,072 µstrain, which was produced by the application of levered bending to metacarpal 4. The mean peak strain rates produced by each technique in vivo are shown in Table 2.
Ex Vivo Testing
The mean compressive strain created by each technique on the metacarpals tested ex vivo is presented in Table 3. A 2-way ANOVA on all ex vivo data demonstrated a difference in the magnitude of strain created between the manual procedures (P <.001). Post hoc testing using a t statistic revealed differences between the manual techniques tested ex vivo. Both shear bending (–1,053 µstrain) and levered bending (–1,395 µstrain) created higher levels of compressive strain than those created by 4-point bending (–594 µstrain) and torsion-rotation (–407 µstrain) (P <.001). Compressive strain magnitude was higher with the procedure of levered bending (–1,395 µstrain) than with shear bending (–1,053 µstrain) (P <.01). No difference was apparent when 4-point bending (–594 µstrain) and torsion-rotation (–407 µstrain) strain magnitudes were compared. The highest mean peak compressive strain produced by the ex vivo application of manual procedures used in this study was –1,884 µstrain, which was created by the application of levered bending to metacarpal 3. The highest peak compressive strain engendered by any of the manual techniques used in this ex vivo phase of the study was –2,079 µstrain, which was created by the application of levered bending to metacarpal 4.
Paired t tests were calculated on each of the manual techniques when performed on the 4 metacarpals both in vivo and ex vivo. No difference was found between the levels of compressive strain that each respective technique could create in vivo or ex vivo. The mean peak strain rates produced by each technique ex vivo are shown in Table 4.
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Discussion
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This study was undertaken as the first step in evaluating the effect of manual procedures on bone and bone cells. The long-term aim of these experiments is to understand the effect of manually applied forces on bone at tissue and cellular levels.
Of the 4 techniques evaluated in this study, only during levered bending and shear bending were compressive strains in excess of –1,000 µstrain. Levered bending was the technique that produced the greatest mean peak strains and greatest peak strains both in vivo and ex vivo. Although no difference was apparent in the magnitude of strain created by levered bending and shear bending in vivo, a difference was evident between the techniques ex vivo (
=–1,395 µstrain for levered bending and –1,053 µstrain for shear bending, P<.01).
All of the techniques in this study resulted in a force manually applied to the midshaft of the bone to produce angular deformation of the bone. The application of levered bending, however, will not only produce compressive strains within the bone but also bending forces, shear forces, and tensile forces. The techniques of 4-point bending, torsion-rotation, and shear bending all result in forces immediately adjacent to the fulcrum. The technique of levered bending utilizes a longer lever arm (approximately 4–5 cm in length) to apply the manual forces onto bone. The longer lever creates a greater force moment at the fulcrum. This force moment engenders a stress gradient along the surface of the bone, with the highest stress gradient being immediately adjacent to the fulcrum. These biomechanical factors give the technique of levered bending a mechanical advantage over the other 3 techniques, and it was obvious that this technique was able to produce the greatest compressive strains created in this study.
The magnitude of compressive strains created in this study has induced osteogenesis in other animal experiments using mechanical devices.5,19,24,25 In one experiment,25 the ability of bone to respond quickly to a change in its mechanical environment was demonstrated when a single episode of compressive loading was applied for 300 load cycles at 0.5 Hz to an avian bony model. Periosteal activation and osteogenesis resulted within 5 days of loading. The magnitude of loading engendered by a mechanical device25 was similar to the levels of compressive strain created by levered bending in the present study. Previous work has demonstrated that compressive strain magnitudes of at least –1,000 µstrain are sufficient to stimulate osteogenesis if applied with an altered strain distribution and with sufficient duration.5
Other researchers have assessed the question of how many load cycles are required to produce a response. As few as 36 load cycles are as effective as 1,800 load cycles in stimulating osteogenesis.24 The techniques used in the current experiments were applied for approximately 30 load cycles. This number of load cycles was chosen arbitrarily as sufficient to obtain a reproducible loading pattern, and operator fatigue did not prevent further loading. It is quite probable that these techniques could be performed for more than 36 load cycles. In the present model, it appears that levered bending can be applied with sufficient magnitude and duration to stimulate osteogenesis.
Application some of the techniques in this study resulted in levels of compressive strain that have been used in other animal experiments to stimulate osteogenesis. It does not necessarily follow, therefore, that the application of levered bending to the ovine 3,4 metacarpal would result in osteogenesis. Factors other than compressive strain magnitude, including the applied loading strain rate and strain distribution caused by the applied load, appear to be important in stimulating osteogenesis.5,18,26,27 Some researchers26,28 have noted that the higher the applied maximum strain rate is, the more osteogenic the stimulus is likely to be. The strain rates created by levered bending in our study ranged between 1,900 and 19,200 µstrains/s. The strain rate produced by physiological activity in experiments on animals have ranged from 4,600 to 122,000 µstrains/s.21,29,30 In the human tibia, strain rates vary from 4,600 µstrain/s during walking to 35,000 µstrain/s during sprinting.30 The strain rate created by levered bending in our study was substantially lower than that created by physiological loading, but it was similar to the strain rate of 10,000 µstrains/s used in previous experiments with animals to stimulate osteogenesis.5,18,25 The similarity between the strain rates of experimental animal studies and manual procedures in our study indicates it is possible that levered bending has a sufficient strain rate that could stimulate osteogenesis.
The strain rate resulting from the applied manual load also has an effect on the resultant strains that the manual load can engender. The faster a specific load is applied to bone, the greater the resultant strain.31 It is possible that loads similar to those used in our study, if applied at a faster loading frequency, may produce faster strain rates and greater levels of compressive strain than those obtained in our study. Further research is needed to clarify the effect of varying the applied manual loading frequency and assessing the resultant compressive strain rate and magnitude.
The ability of an applied mechanical force to stimulate osteogenesis in an area of bone also requires an applied strain distribution that differs from the physiological strain distribution.16–18,24,28,32 In our study, the strain distribution engendered by levered bending onto the surface of the ovine 3,4 metacarpal was unknown. If levered bending is to have the potential to stimulate osteogenesis in this animal model, it must first be proven that the strain distribution produced by this procedure is different from that produced by physiological activities.
Some variance in the levels of compressive strain created by repeat applications of the same technique on the same bone was evident. Body positioning of both operator and subject has been recognized as being important in technique performance.20 The most probable reason for the variance in mean peak strain magnitudes observed could relate to the lack of control of both the applied load magnitude and the loading frequency. Standardization of operator and gauge position allows control only over the moment arm of the technique and not over the magnitude of the load. No load cell or load feedback device was used in the performance of this technique. Previous studies have demonstrated poor intratherapist and intertherapist reliability in estimating the amount of force applied during manual technique performance.33 Thus, it is probable that some of the variance in the levels of compressive strain created by repeat applications of the same technique on the same bone was due to the uncontrolled nature of the loading frequency and the applied manual load.
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Conclusion
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The results of our study show that some of the manual procedures used, in particular levered bending, are able to produce compressive strains that may be of sufficient magnitude to stimulate osteogenesis in the ovine 3,4 metacarpal. This animal model could provide an important insight into the response of skeletal cells and bone matrix to manually applied mechanical forces, particularly if it is possible to stimulate osteogenesis. It remains to be determined whether physical therapists can reliably apply the correct type and level of mechanical forces required to transmit a beneficial and not a detrimental effect on bone metabolism. The effect of different types of manually applied mechanical forces and treatment variables, such as direction of force, loading frequency, duration of stimulus, and frequency of manual stimulation on bone physiology, all remain unclear. Further research on the effect of manually applied force on bone cells in vivo and possibly in vitro will help to determine whether these techniques have any role in the treatment of people with bone injuries.
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Footnotes
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This research received ethical approval from the Animal Experimentation Ethics Committee of the University of Melbourne and the Ethics Committee for Human and Animal Experimentation of La Trobe University.
This study was supported by grants from the Victorian branch of the Australian Physiotherapy Association and the Australian Physiotherapy Research Foundation.
The results of this study, in part, were presented at the Ninth Biennial Conference of the Manipulative Physiotherapists Association of Australia; November 1995; Gold Coast, Queensland, Australia.
* Micromeasurements Group Inc, PO Box 27777, Raleigh, NC 27611. 
B Braun, Melsungen AG, D/3508, Melsungen, Germany.
Du Pont de Nemours & Co Inc, 1007 Market St, Wilmington, DE 19898.
WR & D Wells Pty Ltd, 144 Clarenden St, South Melbourne, Victoria, Australia 3205.
|| Troy Laboratories Pty Ltd, PO Box 6626, Wetherill Park, New South Wales, Australia 2164.
# Analogue Digital Instruments, Unit 6/4 Gladstone Rd, Castle Hill, New South Wales, Australia 2154.
** Arnolds Veterinary Products Ltd, Cartmel Dr, Harlescott, Shrewsbury, Shropshire, England SY13TB.
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Copyright © 1999 by the American Physical Therapy Association.
Top
Introduction
Method
