Effect of pulsed electromagnetic therapy on bone mineral density of female athletes

Background: The prevalence of menstrual irregularities and low bone mineral density (BMD) varies widely in the general population and in the athletic community. Pulsed electromagnetic therapy(PEMT) may stimulate bone formation and prevent bone loss. Objective: The aim of the present study was to evaluate the effect of low-frequency pulsed electromagnetic field therapy (PEMFT) on bone mineral density (BMD) in female athletes. Subjects and methods: A total of 40 female athletes selected from the outpatient clinic of faculty of Physical Therapy, Cairo University, Cairo. Their age was ranged between 15-25 years, BMI: 20-24.9 kg/ m2. They were randomly allocated into two groups: studygroup (A), and the control group (B). The pulsed electromagnetic field therapy (PEMFT) at low frequency 33 Hz and intensity of 50 gauss which equal 60% of the maximum intensity was applied for 30 min, three times weekly for 4 months on the lumbar and hip region for the study group (A). All participants adhered to the calcium and vitamin D medications prescribed by their physicians. BMD was evaluated using dual-energy X-ray absorptiometry for both groups (A&B) before and after treatment. Results: The results revealed a significant increase in BMD of right neck femur and lumber spine (L1-4) in both groups after the treatment program (study group, P<0.001&0.002 and control group, P<0.001&0.001 respectively). Between groups, there were significant differences in BMD of right neck femurand lumber spine (L1-4) but in favor of group A (P<0.001&0.009). The mean values in BMD of Rt neck femur after treatment were 1.021±0.067, 0.959±0.053 in both groups A and B, respectively. The mean values in BMD of lumber spine (L1-4) were 1.044±0.116, 0.970±0.019in both groups A and B, respectively. Conclusion: PEMFT is a useful therapeutic procedure to increase BMD in female athletes


Introduction
The prevalence of menstrual irregularities, eating disorder, and low BMD varies widely in the overall public and in the athletic community [1]. The female athlete triad is a syndrome that has been reported in female athletes with three interrelated components: eating disorder, decreased frequency of menstrual cycle, and osteoporosis [2,3].
Endurance athletes have diminished levels of sex hormones, which may cause physiologic changes that enhance bone loss. This may cause relative osteoporosis despite the loading of the bone during exercise, which would regularly increase bone mineral density. Untimely osteoporosis might be irreversible, making athletesprogress toward osteoporosis at a prior age and have a potential risk of fracture later in life [4].
The spectrum of menstrual function ranges from eumenorrhea to amenorrhea. Eumenorrhea is characterized by monthly cycle every 28 days. Amenorrhea classified into primary and secondary subsets; primary amenorrhea is the disappearance of menarche after age 15, and secondary amenorrhea is the stoppage of menses for three consecutive cycles after CrossMark ← Click for updates doi: 10.7243/2055-2386-5-7 menarche. In the female athlete, menstrual function should be assessed and corrected if it is abnormal because estrogen has an important role in bone wellbeing and remodeling [5].
The diminished rate of bone building in adolescent athletes is especially concerning, since bone mass gains during childhood and adolescence are critical for the attainment of maximal peak bone mass and prevention of osteoporosis in adulthood [6,7].
The established interventions for osteoporosis are pharmacological, which fall in two categories, i.e., enhancing bone formation and inhibition of bone resorption, but each have their own adverse effects [8,9]. Because of these undesired consequences of drug applications, alternative methods have been investigated for a long period of time. One of the therapeutic physiotherapy modality proposed to be a safe and effective is pulsed electromagnetic field [10].
Pulsed electromagnetic field (PEMF) has been proved to improve bone biomechanical properties, prevent bone mass loss, and prevent bone microarchitecture decay [11]. PEMFs may stimulate bone formation, possibly by enhancing osteoplastic activity, in postmenopausal women with osteoporosis [12].
It is generally accepted that optimizing vitamin D and calcium intake in young women is necessary for bone health; particularly vitamin D levels are frequently observed to be low in this age group [13].
Calcium and vitamin D are inexpensive therapies which enhance bone health. Calcium is essential for bone formation and is lost from the body through urine and the renal system every day, and needs to be replaced. Low serum calcium leads to increased parathyroid hormone and increased bone loss. Therefore, maintaining adequate calcium intake is important. Vitamin D is essential for bone health. It is integral to calcium homeostasis and increases intestinal absorption of calcium [14].

Subjects and methods
This study is a prospective, randomized controlled study. Sixty female athletes who had a previous history of participation in Organization and athletic events for at least 3 years (age:15-25 years, BMI :20-24.9 kg/m 2 ) were contacted for this study. Eight of them didn't wish to participate in the study and nine were not fulfilling inclusion criteria and therefore couldn't be included in the study.43 women gave their informed consent to participate in the study. The forty three remaining women were randomly allocated into two groups: study group (group A; n=22), and the control group (group B; n=21). Three had moved away long distance and were unable to attend for bone mineral density (BMD) measurement, so only forty patients were available for post treatment assessment Figure 1.
All of the participants were oligomenorrheic, who had 4-9 menstrual cycles in the last year. They were selected fromout patient clinic of faculty of Physical Therapy, Cairo University to participate in this study. Exclusion criteria were smoking, any pelvic pathology, respiratory diseases like asthma (chronic use of steroids), diabetes, thyroid diseases, cardiac pacemakers, pregnancy, metal implants with ferrous (iron) component, oral contraceptives or any hormonal treatment in the previous six months.
Sample size was calculated on the basis of an estimated large Cohen effect size (F=0.53) using 95% power and 5% significance level that determined a realistic sample size of 40 participants for this study [15].
Patient randomization was reported by physical therapist who did not belong to the study. Reported patients were randomly assigned into either PEMFT group (study group A) or the control group (B) by using the computer generated random numbers. Allocation was concealed in sequentially numbered opaque envelopes. An independent person who was blinded to the research protocol involved in the trial operated the random assignment. All participants adhered to the calcium and vitamin D medications prescribed by their physicians. All females were havinga balanced nutritional diet(adequate protein, carbohydrate and fat intake). All patients were given full explanation of the treatment protocol, and signed informed consents were obtained before participation. This study was approved by the Ethics Committee for Scientific Research of the Faculty of Physical Therapy, Cairo University.

Evaluation
All participant females underwent the same evaluation procedure. The main evaluated parameters were BMD of the lumbar spine (L1-L4) and right femur in mg/cm 2 evaluated using (DXA, Lunar DPX -IQ software version 4.7, Lunar CO,Wi USA). Evaluations of BMD using DXA were performed before and after completion of the treatment program by a specialized physician who was blinded to the study. Demographic doi: 10.7243/2055-2386-5-7 data including age(Years) and BMI (weight kg/m 2 ) were all recorded before treatment.

Pulsed electromagnetic field therapy(PEFT) for study group(A)
Automatic PMT Quattro PRO PEMF device was applied at low frequency 33 Hz and intensity of 50 gauss which equal 60% of the maximum intensity with the rectangular waveform supplied by the applicators. The participant was positioned in a comfortable supine position while wearing light cotton clothes. After properly cleaning the skin with alcohol, the solenoids were adjusted and positioned under the lumber-hip region 30 min/session, 3 sessions/week for 16 weeks.

Supplementation of vitamin D and Calcium for both groups
Both groups received 1200 mg of calcium and 1000 IU of vitamin D dailyfor 16 weeks as prescribed by their physician [16].
Statistical analysis was conducted using SPSS for windows, version 19 (SPSS, Inc., Chicago, IL). Normality test of data using Shapiro-Wilk test was used, that reflect the data was normally distributed for all dependent variables, so parametric analysis was used. Results are expressed as mean±standard deviation. Comparison between variables measured pre-and posttreatment in the same group was performed using paired t test. P value ≤0.05 was considered significant.

Physical characteristics for both groups (A&B)
The demographic characteristics of both groups (A&B) at baseline (age and BMI) revealed no significant differences between the two groups before treatment Table 1.

BMD of right neck femurpre-and post-treatment for both groups (A, B)
BMD(mg/cm 2 ) of Rt neck femur before and after treatment for both groups (A and B) revealed statistically significant increases in BMD for both groups (A&B) after treatment (1.021±0.067, 0.959±0.053 mg/cm 2 ) compared to its corresponding value before treatment (0.943±0.073, 0.935±0.064 mg/cm 2 ). Comparison between both groups (A) and (B), revealed a statistically non-significant difference in BMD of Rtneck femur before the treatment (F=0.155&P=0.696) and a statistically significant

BMD (mg/cm 2 ) of lumber spine (L1-4)pre-and posttreatment for both groups (A&B)
BMD of lumber spine before and after treatment for both groups (A and B) showed statistically significant increases in BMD for both groups (A&B) after treatment (1.044±0.116, 0.970±0.019mg/cm 2 ) respectively compared to its corresponding value before treatment (0.951±0.068, 0.943±0.019 mg/cm 2 ) respectively. Comparison between both groups (A) and (B), revealed a statistically non-significant difference in BMD of lumber spine before the treatment (F=0.223&P=0.640) and a statistically significant difference after the treatment in favor of group (A) (F=7.608&P=0.009) Table 3.

Discussion
Amenorrhea is common infemale athletes, especially those participating in sports, others experience it because of chronically deficient caloric intake that does not compensate for energy expenditure. Complications associated with amenorrhea include decreased peak bone mass in adolescence, and increased therisk of stress fractures [17]. A study by Drinkwater et al. [18] compared lumbar spine bone mineral density (BMD) between eumenorrheic athletes and amenorrheic athletes. Vertebral mineral density was significantly lower in the amenorrheic group than in the eumenorrheic group. So, this study was carried out to determine the Effect of PEMFT on bone mineral densityin female athlete.
This study revealed significant increase in BMD in the study group,this was supported by He et al., [19] who proved that, PEMF may be very effective for bone mass maintenance in subjects with osteoporosis via inhibition of osteoclast formation and activation of osteoblasts.
Increased in BMD caused by PEMF may be caused by the actuation of extracellular signal-regulated kinase (ERK), mitogen-activated protein kinase (MAPK) and prostagland in synthesis, which may havea stimulatory impacts on bone [20][21][22]. In vitro studies proved that a variety of growth factors that are necessary for bone metabolism are affected, including bone morphogenetic protein 2 (BMP-2), transforming growth factor beta (TGF-β) and insulin-like growth factor II (IGF-II) [23][24][25].
In contrast,Van der Jagt et al., [30] used in vivo micro CT scanning and could recognize little bone changes in time. Subtle contrasts in the experimental set-up might clarify the differences in study outcomes in the literature. Since PEMF treatment is safe, further experimental studies on the effect doi: 10.7243/2055-2386-5-7 of PEMF on bonedensity can better be performed directly on humans, disposing of the potential interpretation issues among animals and humans.
This study revealed significant increase in BMD in the control group (B) who adhered to the calcium and vitamin D medications, in addition to the direct effects on bone, vitamin D has been associated with muscle strength. As vitamin D receptors are found in different tissues, including muscle tissue, their activation leads to muscle protein synthesis. In this way, vitamin D supplements may improve muscle strength, and reduce the danger of falls [31].
The mechanism of the impact of calcium and vitamin D is thought to be related todecreasing bone loss [32]. It is additionally possible that the advantageous impacts of vitamin D in people with high calcium intake resulted from particular impacts of 25 OHD on decreasing parathyroid hormone creation [33] or an impact on local formation of calcitriolin bone cells [34].

Conclusion
PEMFT is a useful therapeutic procedure to increase BMD of female athletes.

Competing interests
The authors declare that they have no competing interests.  A, B). Table 3. Mean values of BMD for lumber spine measured pre-and post-treatment for both groups (A, B).