Efficacy of Low Intensity Pulsed Ultrasound on Bone Mineral

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         Efficacy of Low-Intensity Pulsed Ultrasound on Bone Mineral Density in
                          Osteoporotic Postmenopausal Women
    Ali A. Thabet*, Anwar A. Abeed** Shamekh M. El-Shamy*** and **** Omar F. Helal
    * Department of PT for Obstetrics and Gynecology, Faculty of Physical Therapy, Cairo University.
    **Department of PT for Surgery, Faculty of Physical Therapy, Cairo University.
    ***Department of PT for Disturbance of Growth and Development in Children and its Surgery,
    Faculty of Physical Therapy, Cairo University.
    **** Department of PT for cardiopulmonary disorders and geriatrics

    --------------------------------------------- ABSTRACT-------------------------------------------

       Purpose The aim of this current study was to investigate the effect of low –intensity pulsed
ultrasound on bone mineral density (BMD) of lumbar vertebrae in osteoporotic postmenopausal
women. Methods Thirty postmenopausal women suffer from lumbar vertebrae osteoporosis were
selected from Umm El Masryeen General Hospital received ultrasound therapy three time / week for
six weeks. DXA was used for assessment of BMD before and after treatment. Results The results of
the study demonstrate highly significant increase in lumbar BMD. Conclusion It was concluded that
is effective modalities in increasing bone mineral density (BMD) of lumbar vertebrae in osteoporotic
postmenopausal women.

    Key words: Postmenopausal, Bone Mineral Density ,Low-Intensity Pulsed Ultrasound

                  INTRODUCTION                                   ordinary treatments already in existence17.
                                                                 Recently postmenopausal osteoporosis has

O   steoporosis is a metabolic bone disease charac-
    terized by low bone mass, which increases the
                                                                 become an area of interest in terms of medical,
                                                                 social and economic costs35. It is a significant
    bone fragility and the risk of fracture.17 More              cause of women's morbidity and mortality
    cancellous than cortical bone is lost following              leading to fractures of the hip, spine and wrist.
    the menopause due to bone trabeculae being                   Osteoporosis is a primary metabolic disease of
    more sensitive to estrogen deficiency than                   bone and a major public health problem that
    cortical bone, leading to a loss of connectivity             mostly occurs in the elderly23.
    and an increase in its porosity4. Bones, such as
    proximal     femur,     distal   radius    and     the       It       has     been reported that there is
    vertebrae, are composed of a large amount of                 disproportionate loss of trabecular bone from
    trabeculae bone. Thus, treatments to prevent or              the axial skeleton about 47% throughout life
    to stabilize the osteoporosis are important35.               depending on the peak bone mass20. It was
    Alternative treatments are options for those                 reported in the literature that peak bone mass
    people with an increased risk of osteoporosis                in the human skeleton is achieved in the third
    development but with restrictions for the                    to fourth decade of life. However, the adult

skeleton is undergoing a continual process of            intake, smoking, high caffeine consumption
remodeling in which bone resorptions is                  and steroid therapy4.
coupled with bone formation20. At each                   Therapy should be directed primary toward
remodeling site (approximately 0.1mm                of   increasing physical activity, reducing the risk of
bone), a stereotyped sequence of events has              falling and secondarily toward stabilizing bone
been described.An initial stimulus activates             mass17. Reversing the osteoporotic process
the remodeling cycle19. Osteoclasts bone                 require therapy in the form of hormonal
resorbing     cells    that   originate   in       the   replacement21. Calcitonin which is peptide
monocytemacrophage cell line, resorb an                  hormone mediator for estrogen action, produce
apparently predetermined volume of bone .                inhibition of osteoclasts activity and therefore
Having completed this task, the osteoclasts              decrease     the     bone     resorption21.   Also
then disappear and are replaced by osteoblasts,          maintaining a high dietary intake of calcium,
which lay down osteoid refilling the cavity24.           vitamin D, reduction of excessive consumption
Mineralization of osteoid completes the repair           of protein and phorphorous are        indicated as
process. In the aging skeleton, however, there is        therapeutic options . Calcium must be given
an imbalance between the resorptive and                  with sodium fluoride to allow mineralization of
formative process27.                                     the new osteoid. Problems with this modality,
      There are two types of osteoporosis, type          include the questions of abnormal bone
I due to a decrease in cumulating estrogens              architecture and the high incidence of side
which affects trabecular bone (especially                effects18.
vertebral bone) and affects females more than                  The impact of physical activity on BMD
males in a ratio of 1:6. Type II, senile                 was established via reducing and/or preventing
osteoporosis, which is age related and occurs in         the volitional bone loss in both recently
cortical and trabecular bone, affects females and        postmenopausal and very elderly women35 .
males in a ratio of 2:1. 21                              The role of electro-therapy in the management
      It is evident that low bone mass is the            of menopausal osteoporosis is very limited in
most potent factor leading to fracture.                  the literature33. It was concluded that pulsed
Estrogen deficiency is well established as a             electromagnetic field has an effect to slow down
risk factor for osteoporosis4. There are several         the bone mass loss in osteoporosis induced by
risk factor reported in the literature which             ovariectomy in rats and clinical application of
accelerate the development of osteopenic                 the same current in women's osteoporosis was
process includes negative calcium balance,               also reported10.
sedentary       life    style,    immobilization,          The ultrasound is a form of mechanical
menopause (surgical or natural), amenorrhea,             energy       which       promotes    local    bone
family history of osteoporosis, high alcohol             microdeformations, as the natural mechanical

incentive, and which is crucial in stimulating              has been hypothesized that US mechanical
the bone formation               . Several studies have     energy may be an osteogenic stimulus18. This
already shown that low-intensity ultrasound is              theory is supported by a growing body of
capable of accelerating the healing of fresh                evidence demonstrating the skeletal effects of
fractures, delayed healing and nonunions                    Further support for a beneficial skeletal effect of
         .Furthermore, recent experimental studies          low-intensity pulsed US has been provided by in
have shown the ultrasound benefits on large                 vivo investigations8. In vivo, the most frequent
bone defects             and on spine fusion129.            application of low-intensity pulsed US is during
However, there are no studies which relate the              fracture repair. In animal fracture models, such
action of low-intensify ultrasound in cases of              US has been shown to facilitate the rate of
osteoporosis without fractures1.                            endochondral bone formation, increasing the
    Ultrasound (US), a high-frequency acoustic              return of bone mineral density (BMD) at the
energy traveling in the form of a mechanical                fracture site.This results in a 38% acceleration in
wave, represents a potential site-specific                  mechanical strength return18. In humans, low-
intervention for osteoporosis12. Bone is a                  intensity pulsed US has been shown to facilitate
dynamic tissue that remodels in response to                 the return of BMD during limb-lengthening
applied mechanical stimuli14. As a form of                  procedures and induce a 30%-38% reduction in
mechanical stimulation, US is anticipated to                the time to union in fresh fractures.When applied
produce a similar remodeling response. This                 to nonunited fractures, the same US has been
theory is supported by growing in vitro and in              shown to stimulate union in >85% of cases27.
vivo evidence demonstrating an osteogenic                   pulsed-wave US at low (<100 mW/cm2) spatial-
effect of pulsed-wave US at low spatial-                    averaged temporal-averaged intensities9.
averaged         temporal-averaged         intensities14.   It was found that low-intensity pulsed US to
Ultrasound        (US)    represents       a   potential    not only prevent femoral neck bone loss in five
intervention for osteoporosis. US refers to a               osteoporotic    bed-ridden    patients,    but   to
high-frequency nonaudible acoustic energy that              increase BMD levels by 8.9%, on average,
travels in the form of mechanical waves . A                 above baseline levels. BMD on the contralateral
mechanical wave is one in which energy is                   nontreated side decreased by 4.0% within the
transmitted by the movement of particles within             same period. This finding suggests an anabolic
the medium through which the wave is                        effect of low-intensity pulsed US on intact
traveling. As these waves travel as a relatively            bone27.
focused beam (typical effective radiating area =            Ultrasound is a biophysical intervention that is
          2 11
5 cm ) . US can be directed onto specific                   capable of generating piezo-electric effects in
regions to exert a local mechanical stimulus19              bone 2, and increasing electric potentials in
Given the inherent mechanosensitivity of bone, it           bone 15 Using 1.27-MHz ultrasound .

METHODS                                                An imaging test that measures bone density (the
                                                       amount of bone mineral contained in a certain
Subjects:                                              volume of bone) by passing x-rays with two
      Thirty    postmenopausal      women      were
                                                       different energy levels through the bone. It is
selected from Umm El Masryeen General
                                                       used to diagnose osteoporosis (decrease in bone
hospital. The criteria for inclusion were as
                                                       mass and density). Also called BMD scan, bone
follows: (a) DXA diagnosis of normal BMD and
                                                       mineral density scan,
osteoporosis in lumbar vertebrae with no evidence
of vertebral compression fractures, (b) age
                                                       (2) Ultrasonic(US) device (Enraf Nonius –
between 51 to 60 years (to avoid inclusion of
                                                       Sonoplus590): was used to deliver low –intensity
older patients with multiple medical problems),
                                                       pulsed   ultrasound     therapy.   The   apparatus
(c)   no   history   of   cancer,   renal   disease,
                                                       provided the following options: 1MHz frequency
gastrectomy, metabolic bone disease or any
                                                       with transducer having an affective radiating area
condition (such as a neurogenic, myopathic or
                                                       of 5.0 cm2. Intensity up to 1.5 W/cm2 in
connective tissue disorder) that could cause
                                                       continuous mode, and up to 3W/cm2 in pulsed
secondary osteoporosis, (d) no intake of any
                                                       mode. Gel was used as a coupling media.
medications associated with accelerated bone loss
(steroids) or any medications affected bone
metabolism (estrogen, calcium, vitamin D, ...etc),
(e) body mass index not exceeding 30 Kg/m2, non
smoker, parity from 1-3 times and led sedentary
life style without participation at any exercise
training during this study, and, (f) had natural
menopause at least 1 year before entry into the
study with no history of ovariectomy.

(l) Dual x-ray Absorptiometry (DXA) (Model
QDR-1000W, Hologic, Inc., Waltham, MA) was
used for the qualitative assessment of BMD in
the vertebral bodies of the lumbar spine for both

Procedures:                                     analytical test included student t-test for
                                                comparing of means between before and
A. Evaluation                                   after treatment. Significant level of 0.05
     Initially a screening test including       was used throughout all statistical tests
careful history taking and gynecological        within this study, P value < 0.05 indicated
examination were conducted for each             significant results. The smaller the P value
subject before entry in this study. After       obtained the more significant was the
that BMD of lumbar spine (L1.-5) was            result.
measured by DXA densitometry. Evaluation
of lumbar BMD was performed before and
after the end of six weeks of treatment.

                                                      In the present study, the response of
B. Treatment
                                                BMD to low intensity pulsed ultrasound
     All subjects in this study underwent
                                                was investigated. The data collected after
20   minutes     US       application,   with
                                                six weeks of ultrasound treatment were
frequency 1MHz and intensity 0.2 w/cm2 ,
                                                compared with the pre treatment.
for each session, three sessions per week
for six successive weeks period of              As revealed from table (1) and figure (1)
treatment. The treatment procedure was          there was a highly statistically significant
explained to all subjects. Skin was cleaned     increase (P>0.0001) in the mean value of
with alcohol to remove fat. During              lumbar T- Score between pre and post
ultrasound application, the position of the     treatment.
subjects was prone lying position with a
pillow under her abdomen. Ultrasound                  As revealed from figure (2) While
therapy was applied to the lumbar vertebrae     comparing     pre   treatment    and   post
(L1-5) using 5 cm ultrasound head.              treatment, the improvement percentage
                                                was 14.40% and statistically difference
C. Statistical analysis                         (P>0.0001) was highly significant
     Descriptive statistics was presented
as mean, standard deviation (SD) and
percentage      for   qualitative    variable

       Table (1): The comparison between pre & post mean values of the T- score

                                                   Imp. %
                    Pre-ttt Post-ttt     MD                  t value    P value   Significance
                       -      -
       Mean                                                                          Highly
                    3.0167 2.5833      -0.4333      14.4     -6.500     0.0001
        SD          9.129 0.3957

    Fig. (1): The mean value of T-score of pre treatment relative to those of post treatment.

    Fig. (2): The improvement % of the mean values of T-score of post treatment.


      The primary problem in postmenopausal with osteoporosis is thought to be enhancement of bone resorption, with
consequent net loss of bone mass as osteoblasts fail to repair the defect completely which increase the risk to fracture. The
basic problem in the remodeling of bone is directly related to the stimulation, multiplication and proliferation of the
extraperiosteal, periosteal and medullar connective tissue that forms reparative blastemas leading to the consolidation of
the bone .
      Dual X-ray absorptiometry was used for assessment of bone density
      The results of DEXA revealed a highly significant increase in lumbar BMD of postmenopausal osteoporotic women
with low intensity pulsed ultrasound compared to pre treatment lumber BMD.
      The process of bone healing or remodeling is very similar to that of soft tissues healing. It would therefore seem
reasonable to suggest that bone healing and/or remodeling might be stimulated by ultrasound which is reported in our results.
Low intensity pulsed ultrasound can be directed onto specific regions to exert a local mechanical stimulus. Given the
inherent mechanosensitivity of bone, it has been hypothesized that US mechanical energy may be an osteogenic stimulus. This
theory is supported by a growing body of evidence demonstrating the skeletal effects of pulsed-wave US at low (<100
mW/cm2) spatial-averaged temporal-averaged in ten
      Ultrasound is capable of producing changes within the cell membrane. This is illustrated by ultrasound’s capacity to
alter cell membrane permeability to ions and to alter cell membrane electrophysiological properties. Ultrasound can cause
an immediate decrease in intracellular potassium content in thymocytes a reversible increase in the intracellular level of
calcium in chondrocytes), and an increase in calcium incorporation into differentiating cartilage and bone cell cultures 24.
      Depending on the cell type, the result of changes in intracellular calcium ions can be synthesis, secretion, or motility
changes, all of which could promote healing 21.
      With respect to bone healing, there are also indications that ultrasound influences the adenylatecyclase cascade in
the cell membranes of osteoblasts24 a finding which is similar to that observed following an application of static
mechanical load27. The changes in the cell membrane may be the most important mechanism by which the ultrasound
signal influences cellular changes and responses24.

It is not clear if these changes are brought about by a direct mechanical deformation of the cell membrane, deformation of
cell receptors, or indirectly as a consequence of cavitation, microstreaming, or a combination of these or other effects27.

      It has been argued that the beneficial effect of ultrasound on bone healing is due to the piezo-electric phenomenon19.
Bone is piezo-electric, which means that electric potentials are produced in bone when it is subjected to mechanical
stress13. Since Wolff’s law basically states that bone remodels according to functional demands, it is assumed that the
stress-generated potentials in bone serve as a signal which controls bone remodeling13.

      Ultrasound is a biophysical intervention that is capable of generating piezo-electric effects in bone2 and increasing
electric potentials in bone Using 1.27-MHz ultrasound with a very low intensity of 0.00383 W cm–2 on bone,2 measured an
electric potential of 64 µV at the ultrasound frequency in vivo13.

Evidence that osteogenesis is stimulated by ultrasound can be found in vitro studies. Osteoblasts can be stimulated to
increase collagen production 7,27 and increase the production of prostaglandin E2, an important bone-healing mediator that

exert different effects on bone cells in the same microenvironments, such as inhibiting mature rat osteoclasts from
resorbing bone and stimulating osteoblasts for bone formation 17.

In summary, ultrasound stimulation of bone healing may be mediated through cavitation, piezo-electric phenomena, and effects on the cell
membrane. This stimulation appears to be multilevel, involving different cell types in and during the healing process. The   particular properties
of ultrasound would create a series of environmental conditions that accelerate the remodeling of bone . It was reported
that osteogenesis has been considered as depending directly on local circulation . Bone develops better in a well
vascularized environment therefore it would be desirable to produce this situation through therapeutic means in order to
achieve faster bone consolidation. The results registered in this study coincide with many research studies investigating
the effect of low intensity pulsed ultrasound on tissue and bone repair in vivo and vitro models and were in agreement and
supporting our finding.

Elbialy et al.11, studied effects of ultrasound modes on mandibular osteodistraction and they found that Earlier stages of
bone healing were enhanced more by continuous, whereas late stages were enhanced more by pulsed

     Daniela and Alberto.,6 who studied the action of low-intensity pulsed ultrasound in bones of osteopenic rats and they
found that the low-intensity ultrasound can interfere in a positive way on osteoporosis as the treated group, sites with recent
bone formation are shown, which indicates more active osteoblasts
     Warden et al.,32 studied Efficacy of Low-intensity Pulsed Ultrasound in the Prevention of Osteoporosis Following
Spinal Cord Injury and they found that alternate doses of US may have beneficial effects on intact bone. These effects are
likely to be restricted to the outer bone cortex.
     Sheng Sun et al., 27 studied in vitro effects of low intensity ultrasound stimulation on bone cells and they found that low
intensity ultrasound treatment may have a stimulatory effect on bone healing processes as the concentration of PGE2 in
the culture medium significantly increased after ultrasound stimulation which stimulate bone cell metabolism.
     Chang et al.,5 who studied cytokine release from osteoblasts in response to ultrasound stimulation, they found that
increase in osteoblasts growth due to mechanical stimulation of ultrasound and enhance osteoblasts population together.

    Monici et al.,19 who studied the effect of low
                                                                          Tsumaki et al.,30 who studied low-intensity pulsed
intensity     ultrasound     stimulation      on     model      of
                                                                          ultrasound accelerates maturation of callus in patients
osteoclastic precursor, they found that ultrasound
                                                                          treated with opening-wedge high tibial osteotomy by
inducing enhancement of the osteoclastic function and
                                                                          hemicallotasis and they found that low-intensity pulsed
impairment of osteoclastic one at the same time makes
                                                                          ultrasound applied during the consolidation phase of
ultrasound a potential tool to counteract osteoporosis.
                                                                          distraction osteogenesis accelerates callus maturation
    Ramas et al.,23 who studied stimulating bone growth
                                                                          after   opening-wedge         high     tibial      osteotomy    by
using piezoelectric ultrasound transducers on the
                                                                          hemicallotasis in elderly patients.
edentulous jaw and they found that ultrasound
activating bone growth through the mechanical stress                      Eung et al.,12 studied         the effects of low intensity
induced by the propagation of ultrasound into the bone.                   ultrasound stimulation on the proliferation of alveolar
                                                                          bone marrow stem cells and they found that the alveolar
                                                                          bone marrow stem cell counts were significantly

increased    that      indicate   low-intensity   ultrasound
stimulation enhanced bone regeneration.                                               References

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 ‫*** قسى ع.ط الضطشاباث يشاحم انًُى وانتطىس ورشاحتها نذي االطفال- كهيت انؼالد انطبيؼً- رايؼت انقاهشة‬
                ‫**** قسى ع.ط اليشاض انباطُت وانًسُيٍ- كهيت انؼالد انطبيؼً- رايؼت انقاهشة‬

  ‫انهذف يٍ هزا انبحج دساست كفاءة انؼالد بانًىراث انصىتيه يُخفضت انشذة ػهً كخافت انؼظاو نذي انسيذاث بؼذ‬
‫إَقطاع انطًج يغ ورىد هشاشه فً ػظاو انًُطقت انقطُيت. اشتشك فً هزة انذساسه حالحىٌ سيذة تؼاَيٍ يٍ هشاشه‬
 ‫فً ػظاو انًُطقت انقطُيت اختيشٌ يٍ يستشفً أو انًصشييٍ انؼاو وتى ػالرهٍ بانًىراث انصىتيه يُخفضت انشذة‬
    ‫حالث يشاث اسبىػيا نًذة ستت اسابيغ .تى تقييى انحالث قبم وبؼذ انؼالد ػٍ طشيق االشؼت انسيُيه انًىردورت‬
‫(ديكسا). وقذ اكذث َتائذ هزة انذساست ػهً كفاءة انؼالد بانًىراث انصىتيه يُخفضت انشذة ػهً صيادة كخافت انؼظاو‬
                  ‫فً انًُطقت انقطُيت نذي انسيذاث بؼذ إَقطاع انطًج يغ ورىد هشاشه فً انؼظاو‬