Effec ts o f Endu rance and Endu rance-streng th Exercise on Renal Func tion in Abdom inally Obese Wom en w ith Renal Hyperfiltration: A Prospec tive Random ized Trial＊

Monika Szulińska, Dam ian Skrypnik, Marzena Ratajczak, Joanna Karolkiewicz, Edyta M?dry, Katarzyna Musialik, Jaros?aw Walkowiak, Hieronim Jakubowski, and Pawe? Bogdański,#

1. Department of Education and Obesity Treatment and Metabolic Disorders, Poznań University of Medical Sciences, ul. Szamarzewskiego 82, 60-569 Poznań, Poland; 2. Department of Internal Medicine, Metabolic Disorders and Hypertension, Poznań University of Medical Sciences, ul. Szamarzewskiego 82, 60-569 Poznań, Poland; 3. Department of Physiology, Biochemistry and Hygiene, Poznań University School of Physical Education, ul. Królowej Jadwigi 27/39, 61-871 Poznań, Poland; 4. Department of Physiology, Poznań University of Medical Sciences, ul. ?wi?cickiego 6, 60-781 Poznań, Poland; 5. Department of Pediatric Gastroenterology and Metabolic Diseases, Poznań University of Medical Sciences, ul. Szpitalna 27/33, 60-572 Poznań, Poland; 6. Department of Microbiology, Biochemistry and Molecular Genetics, Rutgers University, New Jersey Medical School, International Center for Public Health, 225 Warren Street, Room E230P Newark, New Jersey 07103-3535, USA; 7. Department of Biochemistry and Biotechnology, Poznań University of Life Sciences, Dojazd Str. 11, 60-632 Poznan, Poland; 8. Institute of Bioorganic Chemistry, Polish Academy of Sciences, Noskowskiego Str. 12/14, 61-704 Poznan, Poland

Effec ts o f Endu rance and Endu rance-streng th Exercise on Renal Func tion in Abdom inally Obese Wom en w ith Renal Hyperfiltration: A Prospec tive Random ized Trial＊

Monika Szulińska1, Dam ian Skrypnik2, Marzena Ratajczak3, Joanna Karolkiewicz3, Edyta M?dry4, Katarzyna Musialik1, Jaros?aw Walkowiak5, Hieronim Jakubowski6,7,8, and Pawe? Bogdański1,#

1. Department of Education and Obesity Treatment and Metabolic Disorders, Poznań University of Medical Sciences, ul. Szamarzewskiego 82, 60-569 Poznań, Poland; 2. Department of Internal Medicine, Metabolic Disorders and Hypertension, Poznań University of Medical Sciences, ul. Szamarzewskiego 82, 60-569 Poznań, Poland; 3. Department of Physiology, Biochemistry and Hygiene, Poznań University School of Physical Education, ul. Królowej Jadwigi 27/39, 61-871 Poznań, Poland; 4. Department of Physiology, Poznań University of Medical Sciences, ul. ?wi?cickiego 6, 60-781 Poznań, Poland; 5. Department of Pediatric Gastroenterology and Metabolic Diseases, Poznań University of Medical Sciences, ul. Szpitalna 27/33, 60-572 Poznań, Poland; 6. Department of Microbiology, Biochemistry and Molecular Genetics, Rutgers University, New Jersey Medical School, International Center for Public Health, 225 Warren Street, Room E230P Newark, New Jersey 07103-3535, USA; 7. Department of Biochemistry and Biotechnology, Poznań University of Life Sciences, Dojazd Str. 11, 60-632 Poznan, Poland; 8. Institute of Bioorganic Chemistry, Polish Academy of Sciences, Noskowskiego Str. 12/14, 61-704 Poznan, Poland

ObjectiveObesity is associated w ith kidney defects. Physical activity is a key element in the treatment of obesity. The aim of this study was to compare the effect of endurance and endurance-strength training on kidney function in abdom inally obese women.

MethodsForty-four abdom inally obese women were random ized to endurance training or endurance-strength training, three times a week for 3 months. Before and after the intervention, kidney function was assessed by measuring blood creatinine, urine creatinine, and urine album in levels, and the album in-to-creatinine ratio and glomerular filtration rate (GFR) were calculated.

ResultsRenal hyperperfusion was present in both groups before the study. Follow ing both types of physical activity, sim ilar modifications of the investigated parameters were observed, but with no significant between-group differences. Both courses of training led to a significant increase in blood creatinine and a subsequent decrease in the GFR. A significant increase in urine creatinine and album levels, though not exceeding the range for m icroalbum inuria, was not accompanied by any difference in the album in-to-creatinine ratio after endurance-strength training alone.

ConclusionThree months of either endurance or endurance-strength training has a favorable and comparable effect on renal function in abdom inally obese women w ith renal hyperfiltration.

Abdom inal obesity; Renal function; Physical exercise

www.besjournal.com (full text)CN: 11-2816/QCopyright ?2016 by China CDC

INTRODUCTION

T he second most important contributor to the relative risk of developing end-stage renal disease (ESRD) after proteinuria is the body mass index (BMI)[1-2]. The cause of renal disease associated w ith abdom inal obesity is not well understood, but two relevant elements emerge. The first is the presence of obesity-related glomerulopathy (ORG) and the second is the deposition of fat in the kidney w ith an impact on renal hemodynam ics and intrarenal regulation. The exact mechanisms that link abdom inal obesity and renaldamagearecomplexandinclude hemodynam ic changes, inflammation, oxidative stress, apoptosis, and finally renal scarring[3-4].

The prevalence of ESRD in a group of people w ith BMIs between 18 and 24.5 kg/m2is approximately 10 per 100,000; for BMIs ＞40 kg/m2, it increases to 108 per 100,000, independently of blood pressure or the coexistence of diabetes mellitus. ORG is observed in abdom inally obese people, and particularly in individuals with a BM I ＞40 kg/m2. In addition to abdom inal obesity, ORG patients present proteinuria without swelling, normalbum inem ia,andfocalsegmental glomerulosclerosis without nephrotic syndrome[5]. It has been documented that m icroalbum inuria and elevated album in-to-creatinine ratios (ACR) are independent factors for cardiovascular risk and cardiovascular mortality[6-7]. Moreover, the risk of developing m icroalbum inuria is higher in patients w ith metabolic syndrome[8].

To avoid kidney damage in subjects with abdom inal obesity, a combination of weight reduction and waist circum ference reduction w ith the proper control of renal parameters and obesity-relatedcardiometabolicriskfactors, including metabolic syndrome components such as hypertension, diabetes, and dyslipidem ia is required. The standard therapy for abdom inal obesity is based on improving physical activity and diet. It has been also observed that physical activity may have a nephroprotective effect that is not dependent on the decrease in body mass[9-10]. Currently, the optimal model of physical training in the treatment of abdom inal obesity is being discussed. There is scientific evidence for the superiority of m ixed endurance-strength training over endurance training alone in terms of the improvement it produces in parameters such as waist circum ference[11], total body fat percentage, total body lean mass, total body fat-free mass[12], resting diastolic blood pressure, resting systolic blood pressure, and resting heart rate[13]. However, to the best of our know ledge, there is no strong evidence of the superiority of any type of physical training in the treatment of obesity-related abnormalities of kidney function. The aim of this study was to compare the effect of endurance training with that of endurance-strength training on renal function in abdom inally obese women with renal hyperfiltration.

METHODS

Study Patients

There were 163 registered women w ith obesity screened at the outpatient clinic of the Department of Internal Medicine, Metabolic Disorders, and Hypertension, University of Medical Sciences, in Poznań, Poland. Among them, a total of 44 women were enrolled.

The inclusion criteria were subjects who provided w ritten and informed consent; age 18 to 65 years; simple obesity (BMI ≥30 kg/m2); waist circum ference ＞80 cm; content of body fat assessed by electrical bioimpedance ≥33%; and stable body weight in the month prior to the trial (the perm issible deviation was ±1 kg).

The exclusion criteria were subjects w ith diabetes mellitus; a secondary form of obesity (obesity resulting from any underlying disease) or a secondary form of hypertension (hypertension resulting from any underlying disease); poorly controlled hypertension (mean systolic blood pressure ＞140 mmHg and/or mean diastolic blood pressure ＞90 mmHg) during the month prior to the trial or the necessity to modify antihypertensive treatment in the 3 months prior to the trial; a history of coronal artery disease; stroke; congestive heart failure; clinically significant arrhythm ias; malignancy; a history of the use of any dietary supplements in the 3 months before the study; lipid disorders requiring drug treatment in the 3 months prior to the trial or during the trial; abnormal thyroid gland function; serious liver or kidney dysfunction; clinically significant acute or chronic inflammatory process within the respiratory, digestive, or genitourinary tract, or in the oral cavity, pharynx, or paranasal sinuses, or connective tissue disease or arthritis; history of infection in the month prior to the study; nicotine, alcohol, or drug abuse; pregnancy, childbirth, or lactation at enrollment orin the 3 months prior to enrollment; or any other condition that, in the opinion of the investigators, would make participation not in the best interest of the subject, or could prevent, lim it, or confound the efficacy (not allow to receive an objective result) of the study. The occurrence of any of the above exclusion criteria during the trial resulted in immediate cessation of participation in the study. The characteristics of the study groups are presented in Table 1.

Informed consent in w riting was obtained from all subjects. The study protocol was approved by the Ethics Comm ittee of Poznań University of Medical Sciences (registered as case No. 1077/12 w ith supplement No. 753/13). The present study was performed in accordance with the standards of the Declaration of Helsinki in its revised version of 1975 and its amendments of 1983, 1989, and 1996.

Study Design

The study was designed as a prospective random ized trial. Subjects were random ized into two groups, group A and group B, using a random ization list. Each subject had a unique blinded code, and the random ization was performed using the list of codes. Both groups performed 3 months of physical training. Group A underwent endurance training alone while Group B underwent endurance-strength training of comparable exercise volume. Aside from the training, all subjects were instructed to maintain their usual physical activity and diet. At baseline and after 3 months of physical training, blood and urine samples forlaboratoryanalysesweretaken,and anthropometric measurements[14]were performed in both groups.

Anthropometric Measurements

Anthropometric measurements were conducted w ith the subjects wearing light clothing and no shoes.Weight was measured to the nearest 0.1 kg and height to the nearest 0.5 cm. The BMI was calculated as weight divided by height squared (kg/m2). Obesity was defined as a BMI ≥30 kg/m2. Waist circum ference (cm) was measured to the nearest 0.5 cm at the level of the iliac crest at the end of normal expiration[14]. According to European guidelines, in women, a waist circum ference of 80 cm or higher is categorized as abdom inal obesity[15].

Table 1. Characteristics of the Study Groups before the Intervention[14]

Laboratory Analysis

Parameters specific to kidney function are blood creatinine level, urine creatinine level, and urine album in level. The urine creatinine level and urine album in level were used to calculate the ACR as the urine album in level (mg) divided by urine creatinine level (mmol). The ACR is a good indicator of early kidney damage[16]. The blood creatinine level was used to calculate the glomerular filtration rate (GFR). The GFR was calculated from the modification of diet in renal disease formula (GFR-MDRD) and the Cockcroft-Gaultformula(GFR-CG)[16].Blood creatinine and urine creatinine levels were measured w ith the Jaffe reaction. The urine album in level was measured by immunoturbidimetry. Absorption spectrophotometry was used (ADVIA? 1800, Siemens, Berlin, Germany). The accuracy and precision of the technique used to assay these parameters were validated. Reproducibility was checked with a control of human serum and urine (Alab Laboratory?, Poznań, Poland). Measurements were performed usingcommercialkits(SiemensHealthcare Diagnostics Inc.?, Erlangen, Germany).

Dietary and Supplement Intake

At baseline, every 14 days during the intervention, and upon completion of the trial, dietary intake was determ ined on the basis of dietary intake interviews[17]. A modified food frequency questionnaire was used[18]. The level of nutrients in the daily diet was evaluated using a dietetics computer program. The intake of nutrients, the total caloric intake, and caffeine consumption during the study were constant and comparable between the groups. Subjects were instructed not to use any dietary supplements.

Intervention

The 3-month intervention consisted of a physical exercise program of three sessions per week. The women in each group participated in a total of 36training sessions over a period of 3 months. During each session, the exercise was performed in a professional training room under the supervision of a certified fitness instructor and a physician. The women in group A underwent endurance exercise on cycle ergometers (Schwinn Evolution, Schw inn Bicycle Company?, Boulder, Colorado, USA). The exercise sessions consisted of a 5-m in warm-up (stretching exercise) at low intensity (50%-60% of maximum heart rate), a 45- m in exercise session (at 50%-80% of maximum heart rate), 5 m in of cycling without a load, and 5 m in of closing stretching and breathing low-intensityexercise.GroupBunderwent endurance-strength exercise, which consisted of a 5- m in warm-up (stretching exercises) of low intensity (50%-60% of maximum heart rate), a strength component, an endurance component, cycling w ithout a load, and a closing exercise. The strength component involved a 20- m in strength exercise with a neck barbell and a gymnastic ball. Immediately after the strength exercise, the women performed a 25- m in endurance exercise on cycle ergometers (Schwinn Evolution, Schw inn Bicycle Company?, Boulder, Colorado, USA) at 50%-80% of maximum heart rate, 5 m in of cycling w ithout a load, and 5 m in of closing stretching and breathing low-intensity exercise. The heart rate during the training was monitored using Suunto Fitness Solution? devices. Both training programs were comparable in exercise volume and varied only in the nature of the effort. A detailed training program is described in our previous paper[14].Bothexerciseprogramsimprove cardiorespiratory fitness[13].

Statistical Analysis

Data are presented as means±standard deviations (SDs). All calculations and statistics were performedusingSTATISTICA10.0software (StatSoft?, Inc. 1984-2011, Poland). Comparisons between groups were performed using the Mann-Whitney U-test. Wilcoxon's test was used to analyze the statistical significance between variables before and after the 3-month intervention. A P-value of less than 0.05 was regarded as significant. It was calculated that a sample size of at least 16 subjects in each group would yield at least 80% power of detecting an intervention effect that was statistically significant at the 0.05 α level.

RESULTS

In total, 163 subjects were exam ined during the prerandom ization process. Among them, 119 were excluded from the trial for the follow ing reasons: poorly controlled hypertension (49 subjects), history of coronary artery disease (18 subjects), stroke (6 subjects), congestive heart failure (16 subjects), clinically significant abnormal liver function (9 subjects), clinically significant abnormal kidney function (6 subjects), and clinically significant inflammatory process within the respiratory tract (15 subjects). After screening, the remaining 44 subjects were random ized to group A and group B, each consisting of 22 subjects. One subject from group A and five from group B were removed from the trial following random ization because of low attendance during the intervention process (＜70%). In total, 38 subjects completed the trial and underwent analysis (21 from group A and 17 from group B). The compliance ratio was 86.4%.

Prior to the intervention, there were no differences in any of the parameters between groups A and B. After the study, for both endurance training and endurance-strength training, sim ilar changes w ithin the variables were observed, and no significant differences between groups A and B were found. The data for study population before and after the intervention are summarized in Table 2.

Significant and comparable decreases in body mass, BMI, and waist circum ference in the studied population follow ing the 3-month endurance and endurance-strength training program were reported in our previous study (Table 2)[14]. Both training programs led to a significant increase in blood creatinine (P=0.003 for group A and P=0.021 for group B), which resulted in a significant decrease in the GFR as evaluated by the MDRD formula (P=0.005 for group A and P=0.011 for group B) and in the GFR as calculated by the CG formula (P=0.001 for group A andB).Unlikeendurancetrainingalone, endurance-strength training resulted in a significant increase in urine creatinine level and urine album in concentration (Table 3). Nevertheless, the urine album in concentration did not exceed the m icroalbum inuria level. Neither endurance nor endurance-strength training resulted in significant changes to the ACR. A comparison of studied parameters in groups A and B, before and after the intervention, was presented in Table 3.

DISCUSSION

There is little information available on the effect of particular types of physical activity on renalfirst stage of CKD and is a significant pathogenic factor of ORG[25]. In our study, we observed relatively high values of GFR, reaching 130 m L/1.73 m2·m in-1in group A and exceeding 130 m L/1.73 m2·m in-1in group B; this indicates the presence of renal hyperperfusion in studied women. Both exercise programs led to significant decreases in the GFR, as calculated from the GFR-MDRD and GFR-CG formulae. Since the former does not adjust for body mass (unlike the latter), it underestimates the GFR in obese people. For this reason, we used the CG formula for people w ith a BMI ＞30 kg/m2[16]and additionally confirmed the results. As a consequence of the training, we observed a significant decrease in the GFR-CG to less than 130 m L/1.73 m2·m in-1, both after endurance and endurance-strength exercises. These effects are associated with the reduction of hyperperfusion and subsequent ORG risk. Sim ilar results were obtained in the study performed by Bogdański et al. in obese individuals[26]. After 6 months of increased physical activity in patients w ith simple obesity, these authors observed significant decreases in the GFR-CG, BMI, and waist circum ference, and a significant positive correlation between the change in waist circum ference and the change in the GFR-CG[26]. Smekta?a et al., in a study of obese women, also documented significant decreases in the GFR-CG and BM I and a correlation between the BM I and GFR-CG follow ing 3 months of increased physical training combined with a low-calorie diet[25]. Improvements in renal function, in the form of a significant (31%) decrease in proteinuria in patients with nephropathy, were observed in another study after 5 months of low-calorie diet leading to weight reduction[27]. Praga et al. documented an 80% reduction of proteinuria as an effect of 12% body mass reduction in patients w ith impaired renal function associated with obesity, following 1 year of low-calorie diet[28].

In our study, we found an increase in urine album in concentration and urine creatinine level in women following the endurance-strength training, but not the endurance training alone. However, no changes occurred in the ACR in either group. In terms of these parameters, there were also no differences between the studied groups before and after the intervention. Leehey et al. observed a nonsignificant tendency to a decrease in 24-h proteinuria and ACR in seven obese type-2 diabetic patients with CKD follow ing 24 weeks of aerobic training[29]. It has been also found that aerobic exercise decreases m icroalbum inuria in nondialysis CKD patients[30]. In our study, despite the increase, the urine album in concentration did not exceed the m icroalbum inuria range. The increase in the urine album in and urine creatinine levels follow ing endurance-strength training in our study can be explained by postexercise proteinuria (seen particularly after isometric exercises[31]), increased total body lean mass (seen after endurance-strength training alone[14]), and subsequent increased creatinine synthesis[32].

Our study is one of the first attempts to evaluate the effect of endurance and endurance-strength training on renal function in obese women, and to identify obesity as an important risk factor in the development of renal failure.

Study Lim itations

The major lim itation of this study is the relatively small number of study subjects. The main reason for this was the very rigorous inclusion and exclusion criteria. However, these criteria enabled us to select a homogenous group of subjects not encumbered by diseases or states that m ight have significantly affected the results of the study.

Study Strengths

It is worth emphasizing that the subjects' compliance ratio was over 85%. Participation in training was also very high, which strongly enhances the credibility of this study. The inclusion and exclusion criteria were very strict, elim inating the effect of disruptive factors, meaning factors that m ight have affected the objectivity of the study. The greatest strength of the study is its comparative character, which allowed a clear result regarding the superiority of one of the forms of training to be drawn. This approach is not present in any previous study.

Conclusions

Our findings demonstrate strong evidence of favorable and comparable effects of 3 months of endurance and endurance-strength training on renal function in abdom inally obese women with renal hyperfiltration. Further studies on a large scale should be considered in order to draw a precise conclusion regarding a clinically relevant, nephroprotective action involving physical activity in obese patients.

DISCLOSURE STATEMENT

The authors indicate no conflicts of interest.

Accepted: October 1, 2016

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Biomed Environ Sci, 2016; 29(10): 706-71210.3967/bes2016.095ISSN: 0895-3988

*The study was supported by the National Science Centre, Poland, Grant No. 2014/13/B/NZ7/02209.

#Correspondence should be addressed to Pawe? Bogdański, E-mail: pawelbogdanski@wp.pl, Tel: 48-502335001.

Biographical note of the Monika Szulińska, born in 1974, female, doctoral degree in medicine, majoring in obesity, hypertension and endothelial function.

July 12, 2016;