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Table of Contents
ORIGINAL ARTICLE
Year : 2021  |  Volume : 3  |  Issue : 1  |  Page : 37-45

A study using ultrasonography as an assessment tool to compare the effectiveness of a structured land and aquatic based exercise program on overweight and obese health-care professionals: A randomized clinical trial


Department of Sports Physiotherapy, KAHER Institute of Physiotherapy Belagavi, Karnataka, India

Date of Submission26-Mar-2019
Date of Decision15-May-2019
Date of Acceptance19-Jan-2021
Date of Web Publication31-Jul-2021

Correspondence Address:
Dhaval Chivate
Assistant Professor, Department of Sports Physiotherapy, KAHER Institute of Physiotherapy Belagavi, Karnataka
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/ijptr.ijptr_2_19

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  Abstract 


Context: Overweight and obesity being a health hazard for people of any age and profession requires an effective treatment protocol for weight loss. The benefits of land and aquatic exercises on obesity have been researched individually. Clinical trials are lacking where effectiveness of a structured exercise program in water and on land was compared for weight loss on health care professionals.
Aim: The present study aims to compare the effectiveness between structured land and aquatic-based exercises on anthropometric measures, serum lipid level, and body fat.
Settings and Design: A randomized clinical trial was conducted at the tertiary health-care center of Belagavi.
Materials and Methods: Thirty-two overweight or obese health care professionals were recruited for the study. Participants were divided into two groups, i.e., aquatic and land exercise group. An exercise program for 6 days a week for 3 week was performed. The study outcomes included were ultrasonographic assessment of abdominal obesity along with blood triglyceride and cholesterol levels.
Statistical Analysis used: SPSS Version 23.0 was used for analysis. Pre and post data were compared and analyzed using paired t-test.
Results: Statistically significant reduction in body fat percentage with respect to anthropometric measurements, serum lipid levels, and fat thickness was observed in both the groups. However, there was a greater change in the mean difference of the aqua group as compared to the land group which suggests structured exercises in water are more effective than on land.
Conclusions: The current study concludes that a structured exercise program for 3 weeks in water for overweight and obese health-care professionals showed better outcomes compared to land exercises.

Keywords: Aquatic exercises, Circuit training, Land exercises, Obesity, Overweight, Ultrasonography imaging, Weight loss


How to cite this article:
Chivate D, Gandhi M, Mendes G, Gosavi S. A study using ultrasonography as an assessment tool to compare the effectiveness of a structured land and aquatic based exercise program on overweight and obese health-care professionals: A randomized clinical trial. Indian J Phys Ther Res 2021;3:37-45

How to cite this URL:
Chivate D, Gandhi M, Mendes G, Gosavi S. A study using ultrasonography as an assessment tool to compare the effectiveness of a structured land and aquatic based exercise program on overweight and obese health-care professionals: A randomized clinical trial. Indian J Phys Ther Res [serial online] 2021 [cited 2021 Oct 21];3:37-45. Available from: https://www.ijptr.org/text.asp?2021/3/1/37/322915




  Introduction Top


As defined by the World Health Organization “Overweight and Obesity are defined as abnormal or excessive fat accumulation that may impair health.”[1] India ranks third in the world with a maximum number of people suffering from overweight or obesity, which is caused due to a complex interplay of numerous factors which include biological causes, genetic factors, psychological, environmental, social, and cultural factors.[2],[3],[4] This leads to numerous comorbidities such as complications of the cardiovascular, respiratory, endocrine, musculoskeletal system as well as psychological disturbances.[5],[6] A common trait seen in Indians, 18 years and above, particularly young adults such as medical students, is a nutritional transition to fast food dietary habits from a typical carbohydrate diet.[7] For Asian population, the body mass index (BMI) cutoff for overweight is 23.0–24.9 kg/m2, while that for obesity is >25.0 kg/m2.[8]

According to ACSM guidelines, a minimum requirement of 60 min/day would be sufficient when relying on exercise alone for weight loss.[9] Land-based and aquatic-based exercises given in the form of circuit training protocols have proven to be effective in the prevention of weight gain, initial weight loss of the entire body as well as in isolated body segments along with weight maintenance.[10] However, there continues to be a dearth of knowledge on the effects of a structured exercise program comparing the beneficial effects observed through a land- or aquatic-based exercise protocol performed on overweight and obese health-care professionals.

Land-based form of exercises has proven to be effective in the prevention of weight gain, initial weight loss, and in weight maintenance. However, the unique hydrodynamic properties of water are also effective as well as enjoyable for overweight and obese individuals. Aquatic exercises assist in supporting the body weight thereby reducing the musculoskeletal stress as compared to traditional weight-bearing physical activities. The higher specific heat of water along with its thermoregulatory characteristics permits efficient heat dissipation and yields greater progression in the training intensity or duration as compared to land-based exercises in overweight and obese individuals. Due to this, they suffer from lesser heat stress.[11]

Ultrasonography imaging has proven to be effective and is considered to be as reliable as a dual X-ray absorptiometry in measuring the subcutaneous fat thickness.[12],[13] Various anthropometric measurements such as BMI and waist–hip ratio (WHR) are considered to be a quick screening measure for assessment of obesity. Literature has reported that overweight and obese subjects have substantially higher serum lipids relative to individuals of underweight or average weight and are thus considered a good predictor for obesity.

Overweight and obesity is one of the health hazards for people of any age and profession that requires an effective and efficient treatment protocol to curb its progress. Previous literature has stated the beneficial effects of land and aquatic exercises on obesity and has been researched individually. There is a paucity of evidence available on the effect of structured exercise protocol using land and water-based exercise protocol for overweight and obese health-care professionals; the current study aims at evaluating the effectiveness of land- and aquatic-based exercises on serum lipid levels and fat reduction levels and also to compare the effectiveness between the land and aquatic exercises on the similar components.


  Materials and Methods Top


The study was a randomized clinical trial on overweight and obese health-care professionals. The study was approved by the Institutional Research and Ethics Committee. The trial is registered with the Clinical Trial Registry-India (CTRI/2020/05/025042). Written informed consent was obtained from all the subjects who were recruited for the study.

Obese and overweight health-care professionals between the age group of 18 and 25 years were screened for inclusion and exclusion criteria. Individuals were informed about the aims and procedure of the study and were included if the range of BMI was between 23.0 and 24.9 kg/m2 (overweight) and 25.0–29.9 kg/m2 (obese). Individuals were excluded if they gave a history of exercise-induced asthma, presence of open wound or hemorrhage, use of ongoing medications that would affect the lipid metabolism, menstruation, history of gastrointestinal infection, and hydrophobia.

The sample size calculated was 32, based on the previous literature considering effect size with α value 0.05 and β value 0.80.[14] Subjects were randomly allocated into two groups using lottery method with 16 subjects in each, namely Group A, i.e., aquatic-based circuit exercise program, and Group B i.e., land-based circuit exercise program. All subjects were informed about the purpose of the study at the beginning of their intervention [Figure 1].
Figure 1: Consort chart

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The outcome measures used in the current study were BMI Kg/m2, WHR, subcutaneous fat thickness, and complete lipid diagnostic test.

The BMI was measured at baseline and on completion of the program which was calculated using the formula weight (kgs) divided by height2 (meter). The weight and height were measured using a calibrated weighing scale and a stadiometer to the nearest 0.5 kg and 0.5 cm, respectively, with the subject lightly dressed and barefooted.

For WHR, a standard measuring tape was used to measure the waist circumference (midpoint between the lower margin of the last palpable rib and the top of the iliac crest) and hip circumference (around the widest portion of the buttocks). The measurement was taken during the end of a normal expiration with the participant in a standing position. The two values were divided and a ratio was obtained which was compared with the standard values.

A certified radiologist performed the instrument-assisted ultrasonography imaging. The subjects were made to lie on the assessment couch. They were then draped such that only their abdominal region was visible. The measurements were taken before and after the intervention. The two sites used to measure the thickness were the supraumbilical and infraumbilical regions. The measurement was done from the epidermal layer to the point just above the rectus abdominis aponeurosis and it was recorded in cm [Figure 2].
Figure 2: Subcutaneous fat thickness measurement using instrument assisted ultrasonography

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To associate the risk of developing any metabolic disorders with overweight and obesity, the lipid profile of all the participants was recorded. The total cholesterol and triglyceride levels were recorded before the commencement of the exercise program. Similar recordings were made following the intervention.

[Table 1] indicates exercise and dosage, along with exercise progression for both the study groups.
Table 1: Exercise chart

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In the current study, common tailor-made exercise protocol was given to the subjects in the aquatic exercise group [Figure 3] and also to the subjects in the land exercise group [Figure 4] for a duration of 3 weeks, 6 sessions per week with a progressive increase in the intensity, respectively.[15] The intervention was administered in a swimming pool and fitness center for the aquatic and land groups, respectively. The temperature of the water was between 20° and 25° during the course of the training program. The target heart rate of each subject was calculated using Karvonen's Formula to set the intensity of exercise. The target heart rate was 95.6–121.2 beats/min for the given population and the intensity was maintained at 50%–60% of heart rate maximum according to ACSM criteria for moderate to high-intensity exercises.
Figure 3: Aquatic circuit training exercise

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Figure 4: Land circuit training exercises

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The participants performed a warm-up session of 5 min prior to the intervention which consisted of the upper limb and lower limb stretching where each stretch was maintained for 30 s for 3 repetitions each along with spot jogging for a minute.

Statistical analysis of the present study was done using the The Statistical Package for the Social Sciences software version 23.0 (SPSS for windows, Armonk, NY: IBM corp,USA) to verify the results obtained. Normality distribution was assessed using the Kolmogorov–Smirnov test. Comparison of the difference in pre- and post-between the groups was done by paired t-test. P < 0.05 was considered statistically significant.


  Results Top


The mean age of the subjects in Group A was 23.0093 ± 0.89 years and in Group B was 22.62 ± 1.20 years [Table 2] which showed to be homogeneous.
Table 2: Summary of the demographic data and the baseline characteristic

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There was a statistically significant difference in the values of the mean difference of aqua (1.7263 ± 0.34999) and land (0.4500 ± 0.14142) groups when compared for between- and within-group analysis with respect to BMI using paired sample t-test. However, P value for both groups was 0.001. The mean difference of between- and within-group comparison of aqua (0.0431 ± 0.01662) and land (0.0331 ± 0.02701) group, respectively, with respect to WHR of the subjects in the study is illustrated in [Table 3]. The values obtained clearly interpret a greater reduction in the WHR of subjects in the aqua group compared to that of the land group.
Table 3: Comparison of within and between the two study groups with respect to body mass index and waist hip ratio

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The values of mean differences with respect to reduction in fat percentage at supra- and infraumbilical level using ultrasonography imaging are presented in [Table 4]. The within-group mean difference of supraumbilical region for aqua (0.2500 ± 0.08165) and land (0.1187 ± 0.11087) group shows a greater reduction in fat percentage in the aqua group compared to land group. Similarly, for infraumbilical region the mean difference of aqua (0.2312 ± 0.10145) and land (0.1312 ± 0.08732) showed a significant improvement in the aqua group compared to the land group. However, the between-group analysis of the supraumbilical area for both the groups was found to be significant with P value 0.001. The between-group analysis of infraumbilical area for both the groups was also found to be significant, with P value 0.006.
Table 4: Comparison of within and between the two study groups with respect to supra- and infraumbilical using ultrasonography

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The mean differences of the total cholesterol levels and triglyceride levels of the subjects in the aqua and land groups, respectively, are analyzed and presented in [Table 5]. The within-group mean difference in total cholesterol levels showed a significant improvement in the aqua group (10.5625 ± 5.68001) as compared to the land (5.4375 ± 2.15928) group. Similarly, there was a statistically significant difference in the mean difference in triglyceride levels in the aqua (18.8750 ± 12.48399) group as compared to the land (10.5625 ± 4.24215) group. These values conclude that there was a greater reduction in body fat in the aqua group compared to the land group when given a structured exercise training program.
Table 5: Comparison of within and between the two study groups with respect to total cholesterol and triglycerides levels

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  Discussion Top


The present randomized clinical trial was performed to evaluate the efficacy of a standardized land- and aquatic-based exercise regimen on overweight and obese health-care workers. This research has been undertaken to raise awareness of obesity and its potential complications.

The results of the statistical analysis showed that, relative to the group receiving land workouts, the group receiving standardized water exercise programs showed a marginally better reduction in their body weight in terms of WHR, body fat percentage, and triglyceride levels. The mean age of subjects included in this study ranged from 22 to 24 years because, according to Ferguson, Asian Indians represent a common characteristic of a nutritional change from a traditional carbohydrate diet to fast-food dietary habits, which essentially involves young adults 18 years and above studying in different educational fields.[7] This transition in dietary habits puts younger adults at the risk of developing overweight and obesity.

It has been reported that overweight and obese subjects have comparatively higher serum lipids and percentage of body fat when compared to underweight or average weight individuals and thus becomes a better predictor of obesity following the gold standard measures to assess overweight and obesity. The amount of percentage change in body fat and the changes in the total cholesterol and triglyceride levels in the current study were measured using ultrasonography and serum blood lipid profile as a primary outcome for assessment.

In a study performed by Nikkilä et al., aerobic fitness along with a fitness program shows positive effects on blood cholesterol levels. The primary reason could be an increase in the lipoprotein lipase activity secondary to exercising, thereby breakdown of triglycerides is accelerated, resulting in the transfer of cholesterol and other substances into high-density lipoprotein.[15] This justifies the relative changes in the mean differences in total cholesterol levels and levels of triglycerides in the blood post 3 weeks of structured exercise intervention in land and water performed in the current study.

The current study showed a decline in the BMI and WHR after the 3 weeks of organized circuit exercise activity in land and water. The explanation for this reduction may be similar to Meredith-Jones et al.'s report. According to Meredith-Jones et al., moderate-to-high circuit training exercises help to reduce body fat as there is a decrease in leptin levels and an increase in ghrelin levels that send negative feedback and increase the secretion of dietary hormones from the hypothalamus.[16] According to a recent study, the aerobic capacity of an obese individual can be improved using a circuit-based deep water running program.[17] There were similar responses seen in the subjects performing exercises in the aquatic group in the present study. This was displayed by their ability to perform the circuit exercises with a shorter rest interval between sets as compared to the participants in the land exercise group. This, in turn, led to the increased number of durations of the exercises performed by the participants in each successive week in the aquatic group as compared to the land group.

Circuit training is a form of body conditioning or endurance or resistance training using moderate to high intensity. According to ACSM guidelines and the new perspective study, it is essential to increase the energy expenditure in a weight loss program.[18] In the present study as per the ACSM guidelines, a structured circuit training exercise program was formed and practiced by the overweight and obese health-care professionals for 6 days a week for 3 consecutive weeks. The 3-week circuit training program helped in increasing the lipid metabolism by breaking the fat molecules and in turn decreasing the insulin resistance in the blood. This confirms the use of a circuit training program in the reduction of body fat along with its positive effects on serum lipid levels.[19]

Studies claimed that higher intensity exercises have been successfully used in mobilizing abdominal fat. The mechanism for this is mediated by inducing the secretion of lipolytic hormones, favoring a large negative energy expenditure as well as facilitating greater postexercise energy expenditure along with fat oxidation.[20]

The prevalence of sustaining injuries such as sprains, strains, dislocations, falls as well as lower extremity fractures increase with increasing BMI and high-intensity unstructured, unsupervised exercises.[21] The latest research aimed at using a standardized circuit training program in the land as well as in water for overweight and obese health-care professionals where the postintervention statistical analysis revealed that the group performing water exercises showed better results change compared with the land group. The primary reason could be an increase in the aerobic capacity of the subjects in water in conjunction with an increase in caloric expenditure. Another reason could be the properties of water and the depth of immersion of the subject in the water while performing the exercises.

According to de Goeij and Honkoop along with the increase in the aerobic capacity, the water depth also influenced the energy expenditure. Deeper immersion affected by the physical properties of water which include buoyancy and viscosity as well as the control of movements affect the caloric expenditure which was visible in the participants in the current study as well.[22] The depth of immersion also governs the off-loading of body weight. By immersing the subjects in shoulder-deep water, around 85% of bodyweight depending on the position of arms was off-loaded.[23] This property negated the effects of injuries associated with increased BMI and high-intensity training which was particularly used in this study.

Exercising is viewed as a safe and pleasant fitness experience in an aquatic environment.[24],[25] The perception of exercise benefits increased among the participants in the aquatic training group, because exercising in water reduced the embarrassment which was faced by obese and overweight subjects while performing exercises on land and thus increased the zeal and enthusiasm in each successive session.[26],[27] Therefore, involvement in aquatic therapy resulted in higher weight loss along with beneficial effects on blood cholesterol and triglyceride levels among overweight and obese health-care workers.

The limitations of this study include the defined dietary changes that were not documented. The availability of a medical professional/expert in carrying out the necessary diagnostic procedures and the unavailability of a temperature-controlled pool for aqua therapy sessions were a continuous dependence.

The future scope of the present study is that the circuit training exercise program in water can be conducted in a temperature-regulated aqua therapy pool. This will also incorporate all the beneficial effects of exercising in a heated pool on fat reduction and metabolic activities in the body. The immersion level of the body in the aqua therapy pool can be more markedly defined. Aquatic therapy exercises in conjunction with Pilates can be performed, and a diet plan can be tracked.


  Conclusions Top


Our data suggest that both the intervention groups, i.e., the aqua group and the land group showed a significant reduction in their body weights and in their percentages of abdominal fat thickness as analyzed by the outcome measures which were taken post the 3 weeks of their circuit training exercise intervention. However, a more marked reduction was observed in Group A, i.e., the aqua group as compared to Group B, i.e., the land group which was proven statistically. Hence, the current study concludes that the circuit training exercise program in water for 3 weeks is more effective for weight loss in overweight and obese health-care professionals as compared to the circuit training exercise program on land.

Acknowledgment

We are grateful to the head of the institution for granting us permission to conduct the study and use the research related infrastructure.

Financial support and sponsorship

Nil.>

Conflicts of interest

There are no conflicts of interest.



 
  References Top

1.
Kim SY. The definition of obesity. Korean J Family Med 2016;37:309.  Back to cited text no. 1
    
2.
Kalra S, Unnikrishnan AG. Obesity in India: The weight of the nation. J Med Nutr Nutraceuticals 2012;1:37.  Back to cited text no. 2
    
3.
Wyatt SB, Winters KP, Dubbert PM. Overweight and obesity: Prevalence, consequences, and causes of a growing public health problem. Am J Med Sci 2006;331:166-74.  Back to cited text no. 3
    
4.
Ross SE, Flynn JI, Pate RR. What is really causing the obesity epidemic? A review of reviews in children and adults. J Sports Sci 2016;34:1148-53.  Back to cited text no. 4
    
5.
Kelishadi R. Childhood overweight, obesity, and the metabolic syndrome in developing countries. Epidemiol Rev 2007;29:62-76.  Back to cited text no. 5
    
6.
Guh DP, Zhang W, Bansback N, Amarsi Z, Birmingham CL, Anis AH. The incidence of co-morbidities related to obesity and overweight: A systematic review and meta-analysis. BMC Public Health 2009;9:88.  Back to cited text no. 6
    
7.
Ferguson B. ACSM's guidelines for exercise testing and prescription 9th ed. 2014. J Can Chiropr Assoc 2014;58:328.  Back to cited text no. 7
    
8.
Swift DL, Johannsen NM, Lavie CJ, Earnest CP, Church TS. The role of exercise and physical activity in weight loss and maintenance. Prog Cardiovasc Dis 2014;56:441-7.  Back to cited text no. 8
    
9.
Misra A, Chowbey P, Makkar BM, Vikram NK, Wasir JS, Chadha D, et al. Consensus statement for diagnosis of obesity, abdominal obesity and the metabolic syndrome for Asian Indians and recommendations for physical activity, medical and surgical management. J Assoc Physicians India 2009;57:163-70.  Back to cited text no. 9
    
10.
Colberg SR, Sigal RJ, Fernhall B, Regensteiner JG, Blissmer BJ, Rubin RR, et al. Exercise and type 2 diabetes: The American College of Sports Medicine and the American Diabetes Association: Joint position statement. Diabetes Care 2010;33:e147-67.  Back to cited text no. 10
    
11.
Nagle EF, Robertson RJ, Jakicic JJ, Otto AD, Ranalli JR, Chiapetta LB. Effects of a combined aquatic exercise and walking in sedentary obese females undergoing a behavioral weight-loss intervention. Int J Aquatic Res Educ 2007;1:5.  Back to cited text no. 11
    
12.
Carson PL, Rubin JM, Chiang EH. Fetal depth and ultrasound path lengths through overlying tissues. Ultrasound Med Biol 1989;15:629-39.  Back to cited text no. 12
    
13.
Pineau JC, Filliard JR, Bocquet M. Ultrasound techniques applied to body fat measurement in male and female athletes. J Athl Train 2009;44:142-7.  Back to cited text no. 13
    
14.
de Souza Vasconcelos KS, Dias JM, de Araújo MC, Pinheiro AC, Maia MM, Dias RC. Land-based versus aquatic resistance therapeutic exercises for older women with sarcopenic obesity: Study protocol for a randomized controlled trial. Trials 2013;14:296.  Back to cited text no. 14
    
15.
Nikkilä EA, Kuusi T, Myllynen P. High density lipoprotein and apolipoprotein AI during physical inactivity: Demonstration of low levels in patients with spine fracture. Atherosclerosis 1980;37:457-62.  Back to cited text no. 15
    
16.
Meredith-Jones K, Legge M, Jones L. Circuit based deep water running improves cardiovascular fitness, strength and abdominal obesity in older, overweight women aquatic exercise intervention in older adults. Medicina Sportiva2009; 13:5-12.  Back to cited text no. 16
    
17.
Kang SJ, Kim JH, Gang Z, Yook YS, Yoon JR, Ha GC, et al. Effects of 12-week circuit exercise program on obesity index, appetite regulating hormones, and insulin resistance in middle-aged obese females. J Phys Ther Sci 2018;30:169-73.  Back to cited text no. 17
    
18.
Kyu HH, Bachman VF, Alexander LT, Mumford JE, Afshin A, Estep K, et al. Physical activity and risk of breast cancer, colon cancer, diabetes, ischemic heart disease, and ischemic stroke events: Systematic review and dose-response meta-analysis for the Global Burden of Disease Study 2013. BMJ 2016;354:i3857.  Back to cited text no. 18
    
19.
Kim JW, Ko YC, Seo TB, Kim YP. Effect of circuit training on body composition, physical fitness, and metabolic syndrome risk factors in obese female college students. J Exerc Rehabil 2018;14:460-5.  Back to cited text no. 19
    
20.
Imbeault P, Saint-Pierre S, Alméras N, Tremblay A. Acute effects of exercise on energy intake and feeding behaviour. Br J Nutr 1997;77:511-21.  Back to cited text no. 20
    
21.
Finkelstein EA, Chen H, Prabhu M, Trogdon JG, Corso PS. The relationship between obesity and injuries among U.S. adults. Am J Health Promot 2007;21:460-8.  Back to cited text no. 21
    
22.
de Goeij P, Honkoop PJ. Experimental effects of immersion time and water temperature on body condition, burying depth and timing of spawning of the tellinid bivalve Macoma balthica. Helgoland Mar Res 2003;57:20.  Back to cited text no. 22
    
23.
Torres-Ronda L, Del Alcázar XS. The properties of water and their applications for training. J Hum Kinet 2014;44:237-48.  Back to cited text no. 23
    
24.
Belza B, Topolski T, Kinne S, Patrick DL, Ramsey SD. Does adherence make a difference? Results from a community-based aquatic exercise program. Nurs Res 2002;51:285-91.  Back to cited text no. 24
    
25.
Schelling S, Munsch S, Meyer AH, Newark P, Biedert E, Margraf J. Increasing the motivation for physical activity in obese patients. Int J Eat Disord 2009;42:130-8.  Back to cited text no. 25
    
26.
Wouters EJ, Van Nunen A, Geenen R, Kolotkin RL, Vingerhoets AJ. Effects of aqua jogging in obese adults: A pilot study. J Obes 2009;20:2010.  Back to cited text no. 26
    
27.
Takeshima N, Rogers ME, Watanabe E, Brechue WF, Okada A, Yamada T, et al. Water-based exercise improves health-related aspects of fitness in older women. Med Sci Sports Exerc 2002;34:544-51.  Back to cited text no. 27
    


    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4]
 
 
    Tables

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5]



 

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