Effects of Ultrasound on Bone Marrow
To the Editor: I would like to make comment on and ask for some clarifications of the study entitled "Effects of Therapeutic Ultrasound on Bone Marrow in Dogs" by Payton, Lamb, and Kasey reported in the January issue of Physical Therapy. I feel the study as reported presents a misunderstanding of the application of thera peutic ultrasound. By definition, therapeutic heat is considered to be temperature elevation to within the range of 39 to 45 degrees Celsius. There is no evidence in the literature which indicates that within these limits tissue damage is produced. Also, the safety limit of this range is controlled by the pain tolerance of the patient. Based on information which exists within the literature and our own laboratory experience, the findings reported are likely the result of temperatures which markedly ex ceeded the limits of the therapeutic range. I feel that these findings could not be produced by ultrasound in patients who had intact sensory function. The first comment relates to the statement that "no conclusive evidence could be found in the literature that ultrasound at clinical dosages increased the temperature of bone marrow in vivo." In the second reference cited, 1 ultra sound was applied to the thighs of fifteen live anesthetized hogs with temperature probes placed in the bone and soft tissue (thickness ranged from 2 to 3 cm). The energy was applied at 1.5 watts per square centimeter with a 12.5 square-centimeter transducer using a 10-centi meter stroke at twenty strokes per minute for five minutes. Temperature distributions mea sured in the fifteen animals showed the bone marrow temperature increased a mean of 0.93 degrees Celsius with a variance of 0.23 degrees. In your "pilot study," when you measured temperature elevation in the bone marrow, 534
opinions and comments of readers several points are unclear: 1) Where was the thermistor bead located in relation to the bone chip? 2) What was the orientation of the transducer relative to the area of disrupted bone? 3) What was the method of application of ultrasound, i.e., stationary or stroking technique? In the methods sections of your first and second experiments, you do not indicate whether the animals were anesthetized or sedated during each of the ten treatment sessions. If they were not, it seems questionable that they could tolerate the temperatures produced by sonation at 1.5 or 2.5 watts per square centimeter for five or ten minutes with only a seven to nine millimeter thickness of tissue over the bone, whether a stationary or stroking technique was used. In a study conducted on five unanesthetized humans, deep pain was produced in an average of 2.41 minutes with sonation at 1.5 watts per square centimeter (12.5 cm 2 transducer) using a controlled and precisely directed stroking technique. 2 These subjects had an average of 5.4 centimeters of soft tissue cover over the bone. It is, therefore, inconceivable that the animals in your study could have tolerated energy input at the levels described, if it was directly incident on the bone. In order to fully determine the effects of ultrasonic energy on biologic tissues, the tem perature distributions produced by this energy must be considered. Chan calculated the rela tive heating pattern of ultrasound in a threemedia system of fat, muscle, and bone. 3 He showed that most of the ultrasonic energy is converted to heat at the surface of the solid bone. Based on this information and actual measurements made, the temperatures pro duced in solid bone are significantly higher than those which occur in bone marrow. If the temperature differential measured between bone marrow and solid bone in hogs 1 PHYSICAL THERAPY
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letters to the editor
REFERENCES
1. Lehmann JF: Heating produced by ultrasound in bone and soft tissue. Arch Phys Med Rehabil 48:397-400, 1967 2. Lehmann JF, DeLateur BJ, Warren CG, Stonebridge JS: Therapeutic temperature produced by ultrasound as modified by volume of tissue exposed. Arch Phys Med Rehabil 48:662-666, 1967 3. Chan AK, Siglemann RA, Guy AW: Calculations of therapeutic heat generated by ultrasound in fatmuscle-bone layers. IEEE Trans Biomed Engr, BME-21 4:280, 1974
C. GERALD WARREN Coordinator of Research Department of Rehabilitation Medicine University of Washington, Seattle WA 98195
Dr. Payton and Mr. Lamb respond: In answer to Mr. Warren's specific questions, the thermistor bead was located 4.3 centimeters proximal to the proximal edge of the bone chip and it pointed toward the center of the femur within the marrow cavity. The technique with the transducer was exactly the same in the pilot study as it was in the two experiments described; that is, slow stroking over the Volume 55 / Number 5, May 1975
lateral-distal end of the femur was used so that the center of the area sonated approximated the point where the thermistor bead was located when it was inserted. The area sounded in the pilot study was totally undisturbed by the surgery, which permitted the insertion of the thermistor. Although the main theme of Lehmann's first 1967 article was not concerned with bone marrow, Mr. Warren is correct in that Lehmann does give bone marrow temperature in his first table. Our review of literature would have been more complete had we cited that fact. Never theless, it is our belief that neither Lehmann's report nor ours constitutes a definitive and conclusive statement on the subject. Many of the parameters concerning the influence, or potential influence, of ultrasound on bone marrow are yet to be studied and, obviously, extrapolation from animal studies to human therapeutics must be made with extreme caution. Also, we were concerned With "thera peutic dosages" not "therapeutic tempera tures." We most certainly are not advocating a direct translation of our findings to clinical treatment. The rest of Mr. Warren's letter is highly hypothetical in nature, and since we did not have thermocouples on the surface of the bone, within the cortical bone, or in spongy bone, we can neither support nor deny his hypothetical calculations. However, against his conjectures, we can set our experiences with the unanesthetized animals. During all of the soundings in both the first and the second experiments, the dogs were brought directly from the kennel and treated without anesthesia and essentially with out restraint. The therapist who was sounding the limb held the limb in a stable position while sounding the femur and another therapist petted the dog's head. The petting and personal attention were all the restraints necessary during the treatments. If the dogs indicated any discomfort, the rate of stroking with the sound head was increased. This rate change points to one essential difference between our study and that of Lehmann's. In addition to the fact that Lehmann's animals were anesthetized, he also used a controlled stroke rate. Our procedure was more typical of clinical procedure in that we increased the rate of stroking in response to the subject's reactions. Under the circum535
Downloaded from https://academic.oup.com/ptj/article-abstract/55/5/534/4567682 by University of Texas at Dallas - McDermott Library user on 04 February 2019
is used to infer the temperature differential which may have been produced in dogs, then at 1.5 watts per square centimeter when you measured a 1.8 degree Celsius change in the bone marrow, at least an 8.8 degree change would have occurred in the solid bone. At 2.5 watts per square centimeter, the temperature increase in bone marrow was 5.0 degrees, which would have been accompanied by an increase of at least 24.5 degrees in solid bone. When these temperature increases are added to the baseline data, the final temperatures in the solid bone would have risen to at least 48 degrees and 63 degrees respectively after five minutes sonation. These are not "therapeutic temperatures." In the second experiment in the study, 2.5 watts per square centimeter was applied for ten minutes, which would infer that significant regional destruction may have occurred because of the extreme temperature rise in solid bone. Since such an extreme temperature rise could not occur in a clinical situation, I would suggest that your findings which indicate damage are not relevant to the therapeutic use of ultra sound.
To the Editor: I would like to make comment on and ask for some clarifications of the study entitled "Effects of Therapeutic Ultrasound on Bone Marrow in Dogs" by Payton, Lamb, and Kasey reported in the January issue of Physical Therapy. I feel the study as reported presents a misunderstanding of the application of thera peutic ultrasound. By definition, therapeutic heat is considered to be temperature elevation to within the range of 39 to 45 degrees Celsius. There is no evidence in the literature which indicates that within these limits tissue damage is produced. Also, the safety limit of this range is controlled by the pain tolerance of the patient. Based on information which exists within the literature and our own laboratory experience, the findings reported are likely the result of temperatures which markedly ex ceeded the limits of the therapeutic range. I feel that these findings could not be produced by ultrasound in patients who had intact sensory function. The first comment relates to the statement that "no conclusive evidence could be found in the literature that ultrasound at clinical dosages increased the temperature of bone marrow in vivo." In the second reference cited, 1 ultra sound was applied to the thighs of fifteen live anesthetized hogs with temperature probes placed in the bone and soft tissue (thickness ranged from 2 to 3 cm). The energy was applied at 1.5 watts per square centimeter with a 12.5 square-centimeter transducer using a 10-centi meter stroke at twenty strokes per minute for five minutes. Temperature distributions mea sured in the fifteen animals showed the bone marrow temperature increased a mean of 0.93 degrees Celsius with a variance of 0.23 degrees. In your "pilot study," when you measured temperature elevation in the bone marrow, 534
opinions and comments of readers several points are unclear: 1) Where was the thermistor bead located in relation to the bone chip? 2) What was the orientation of the transducer relative to the area of disrupted bone? 3) What was the method of application of ultrasound, i.e., stationary or stroking technique? In the methods sections of your first and second experiments, you do not indicate whether the animals were anesthetized or sedated during each of the ten treatment sessions. If they were not, it seems questionable that they could tolerate the temperatures produced by sonation at 1.5 or 2.5 watts per square centimeter for five or ten minutes with only a seven to nine millimeter thickness of tissue over the bone, whether a stationary or stroking technique was used. In a study conducted on five unanesthetized humans, deep pain was produced in an average of 2.41 minutes with sonation at 1.5 watts per square centimeter (12.5 cm 2 transducer) using a controlled and precisely directed stroking technique. 2 These subjects had an average of 5.4 centimeters of soft tissue cover over the bone. It is, therefore, inconceivable that the animals in your study could have tolerated energy input at the levels described, if it was directly incident on the bone. In order to fully determine the effects of ultrasonic energy on biologic tissues, the tem perature distributions produced by this energy must be considered. Chan calculated the rela tive heating pattern of ultrasound in a threemedia system of fat, muscle, and bone. 3 He showed that most of the ultrasonic energy is converted to heat at the surface of the solid bone. Based on this information and actual measurements made, the temperatures pro duced in solid bone are significantly higher than those which occur in bone marrow. If the temperature differential measured between bone marrow and solid bone in hogs 1 PHYSICAL THERAPY
Downloaded from https://academic.oup.com/ptj/article-abstract/55/5/534/4567682 by University of Texas at Dallas - McDermott Library user on 04 February 2019
letters to the editor
REFERENCES
1. Lehmann JF: Heating produced by ultrasound in bone and soft tissue. Arch Phys Med Rehabil 48:397-400, 1967 2. Lehmann JF, DeLateur BJ, Warren CG, Stonebridge JS: Therapeutic temperature produced by ultrasound as modified by volume of tissue exposed. Arch Phys Med Rehabil 48:662-666, 1967 3. Chan AK, Siglemann RA, Guy AW: Calculations of therapeutic heat generated by ultrasound in fatmuscle-bone layers. IEEE Trans Biomed Engr, BME-21 4:280, 1974
C. GERALD WARREN Coordinator of Research Department of Rehabilitation Medicine University of Washington, Seattle WA 98195
Dr. Payton and Mr. Lamb respond: In answer to Mr. Warren's specific questions, the thermistor bead was located 4.3 centimeters proximal to the proximal edge of the bone chip and it pointed toward the center of the femur within the marrow cavity. The technique with the transducer was exactly the same in the pilot study as it was in the two experiments described; that is, slow stroking over the Volume 55 / Number 5, May 1975
lateral-distal end of the femur was used so that the center of the area sonated approximated the point where the thermistor bead was located when it was inserted. The area sounded in the pilot study was totally undisturbed by the surgery, which permitted the insertion of the thermistor. Although the main theme of Lehmann's first 1967 article was not concerned with bone marrow, Mr. Warren is correct in that Lehmann does give bone marrow temperature in his first table. Our review of literature would have been more complete had we cited that fact. Never theless, it is our belief that neither Lehmann's report nor ours constitutes a definitive and conclusive statement on the subject. Many of the parameters concerning the influence, or potential influence, of ultrasound on bone marrow are yet to be studied and, obviously, extrapolation from animal studies to human therapeutics must be made with extreme caution. Also, we were concerned With "thera peutic dosages" not "therapeutic tempera tures." We most certainly are not advocating a direct translation of our findings to clinical treatment. The rest of Mr. Warren's letter is highly hypothetical in nature, and since we did not have thermocouples on the surface of the bone, within the cortical bone, or in spongy bone, we can neither support nor deny his hypothetical calculations. However, against his conjectures, we can set our experiences with the unanesthetized animals. During all of the soundings in both the first and the second experiments, the dogs were brought directly from the kennel and treated without anesthesia and essentially with out restraint. The therapist who was sounding the limb held the limb in a stable position while sounding the femur and another therapist petted the dog's head. The petting and personal attention were all the restraints necessary during the treatments. If the dogs indicated any discomfort, the rate of stroking with the sound head was increased. This rate change points to one essential difference between our study and that of Lehmann's. In addition to the fact that Lehmann's animals were anesthetized, he also used a controlled stroke rate. Our procedure was more typical of clinical procedure in that we increased the rate of stroking in response to the subject's reactions. Under the circum535
Downloaded from https://academic.oup.com/ptj/article-abstract/55/5/534/4567682 by University of Texas at Dallas - McDermott Library user on 04 February 2019
is used to infer the temperature differential which may have been produced in dogs, then at 1.5 watts per square centimeter when you measured a 1.8 degree Celsius change in the bone marrow, at least an 8.8 degree change would have occurred in the solid bone. At 2.5 watts per square centimeter, the temperature increase in bone marrow was 5.0 degrees, which would have been accompanied by an increase of at least 24.5 degrees in solid bone. When these temperature increases are added to the baseline data, the final temperatures in the solid bone would have risen to at least 48 degrees and 63 degrees respectively after five minutes sonation. These are not "therapeutic temperatures." In the second experiment in the study, 2.5 watts per square centimeter was applied for ten minutes, which would infer that significant regional destruction may have occurred because of the extreme temperature rise in solid bone. Since such an extreme temperature rise could not occur in a clinical situation, I would suggest that your findings which indicate damage are not relevant to the therapeutic use of ultra sound.
