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Table of Contents
ORIGINAL ARTICLE
Year : 2021  |  Volume : 64  |  Issue : 2  |  Page : 106-114

Effects of moderate intensity endurance training and high-intensity interval training on the reproductive parameters of wistar rats overfed in infancy


Department of Medicine, Postgraduate Health Program, Federal University of Juiz de Fora, Juiz de Fora, MG, Brazil

Date of Submission23-Nov-2020
Date of Decision03-Feb-2021
Date of Acceptance19-Feb-2021
Date of Web Publication28-Apr-2021

Correspondence Address:
Dr. Carlos Gabriel de Lade
Department of Medicine, Postgraduate Health Program, Federal University of Juiz de Fora, Juiz de Fora, MG
Brazil
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/cjp.cjp_96_20

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  Abstract 


Studies indicate that rapid weight gain at critical development stages, such as the lactation period, is associated with the development of obesity, cardiovascular diseases, and diabetes in the long term. In addition to metabolic changes during adulthood, overweight/obesity may influence reproductive function. Human and animal studies suggest that lifestyle changes through exercise and/or controlled diet result in improved semen quality in obese individuals. However, the relationship between exercise volume/intensity and reproductive capacity effects remains inconclusive. The present study aimed to evaluate the effects of moderate intensity endurance training and high-intensity interval training (HIIT) on the reproductive parameters of lactating overfed male Wistar rats. Postnatal overfeeding was induced by applying the litter size reduction method. Forty males Wistar rats were used, divided into four groups: one with control litters (CLs) (10 animals/litter-sedentary) and three with small litters (SLs) (4 animals/litter), divided into sedentary, moderate endurance training, and HIIT. Morphologic, metabolic, and reproductive variables were analyzed. SL sedentary group showed increased body weight, adiposity, and decreased relative weight of the seminal vesicle, prostate, and epididymis as well as changes in the insulin tolerance and oral glucose tolerance tests glycemic tests compared to CL sedentary group. Endurance and HIIT protocols were efficient in improving the glycemic metabolism, central fat accumulation of trained groups and did not affect reproductive parameters. Endurance and HIIT protocols proved to be effective in reversing these metabolic changes without impairing the evaluated reproductive parameters.

Keywords: Aerobic exercise, high-intensity interval training, male infertility, obesity, seminal profile, sperm count


How to cite this article:
Bolotari M, Andreazzi AE, de Lade CG, Goncalves Costa VM, Guerra Md, Peters VM. Effects of moderate intensity endurance training and high-intensity interval training on the reproductive parameters of wistar rats overfed in infancy. Chin J Physiol 2021;64:106-14

How to cite this URL:
Bolotari M, Andreazzi AE, de Lade CG, Goncalves Costa VM, Guerra Md, Peters VM. Effects of moderate intensity endurance training and high-intensity interval training on the reproductive parameters of wistar rats overfed in infancy. Chin J Physiol [serial online] 2021 [cited 2021 Nov 27];64:106-14. Available from: https://www.cjphysiology.org/text.asp?2021/64/2/106/315094




  Introduction Top


The lactation period is considered critical for mammalian development, especially the central nervous system, and excess neonatal caloric intake may play an essential role in the development of obesity and associated complications in adulthood.[1],[2] Moreover, this is a period of significant metabolic plasticity and consequently, exposure to inadequate nutritional stimuli during these phases can affect both metabolism and long-term reproductive capacity.[3]

The litter reduction model (small litter [SL]) has been used to evaluate the effects of early overnutrition on the development of obesity and its risk factors in adulthood, as the reduction in the number of pups during breastfeeding decreases breastfeeding competitiveness, increasing calorie intake by offspring. Lactated overfed animals may develop hyperinsulinemia, insulin and leptin resistance, hyperphagia, increased fat accumulation, and higher body weight, both during infancy and adulthood.[4]

Research involving reproductive capacity assessments has indicated that obese individuals present altered seminal parameters, such as reduced sperm concentration, morphology and abnormal sperm motility, in addition to impaired chromatin integrity.[5],[6]

Human and animal studies suggest that lifestyle changes through exercise and/or controlled diet result in improved semen quality in obese individuals.[7],[8] Ibáñez et al.[9] evaluated the effects of moderate intensity aerobic training on the reproductive parameters of rats fed a high fat diet during adolescence and reported that the adopted training protocol was effective in reversing negative changes in the reproductive parameters of these animals after 4 weeks.

However, the relationship between exercise volume/intensity and reproductive capacity effects remains inconclusive. In a review, Hayden et al.[10] conclude that men undergoing high volumes and training intensities may present alterations in several reproductive parameters, including sperm morphology, concentration and motility, in addition to decreased luteinizing hormone, follicle-stimulating hormone, and testosterone.

Moderate intensity or endurance prolonged aerobic exercise sessions over several weeks increase the oxidative capacity of the skeletal muscle, altering the energy substrate used during exercise and resulting in increased aerobic capacity. However, recent studies have demonstrated that high-intensity interval training (HIIT) alters the skeletal muscle energy metabolism and resembles adaptations caused by moderate intensity aerobic training.[11],[12]

The benefits of exercise on obesity prevention and control are well reported in the literature. However, a gap regarding the possible deleterious effects of high training intensities on reproductive parameters is noted. Furthermore, the effects of the intensity of different types of physical training initiated during infancy on possible reproductive changes caused by metabolic changes in overfed lactating Wistar rats have not been investigated. Thus, the aim of the present study was to evaluate the effects of moderate intensity endurance training and HIIT on the reproductive parameters of lactating overfed male Wistar rats.


  Materials and Methods Top


Animals

Twelve pregnant Wistar females were obtained from the breeding facility belonging to the Reproduction Biology Center of the Federal University of Juiz de Fora (CBR/UFJF), CIAEPE 02.0048.2019. A total of 40 males bred from these females were used in the experiment. On the 2nd postnatal day, the animals were divided into two groups: Control Litter Group (CL; ten animals/litter) and Small Litter Group (SL; four animals/litter) to comprise the experimental groups after weaning. Litter reduction was performed on the 2nd postnatal day, according to Bei et al.,[13] as well as animal relocation for the formation of litters composed exclusively of male pups.

The animals were kept in air-conditioned ALESCO® shelves under standard humidity and ventilation laboratory conditions, at a temperature control of 22°C ± 2°C and a 12 h light/dark photoperiod, housed in cages (3–4 animals/cage). After weaning (21st postnatal day), the animals were fed standard animal feed pellets (NUVILAB CR1®, Nuvital Nutrientes Ltda. Colombo, Brazil) and filtered water ad libitum. All adopted procedures were approved by the Animal Use Ethics Committee of the Federal University of Juiz de Fora (CEUA/UFJF), under protocol 045/2015.

Experimental groups

At weaning, SL animals were randomly assigned to three experimental groups: sedentary (SLSed), endurance (SLEnd) and HIIT (SLHIIT), while CL animals were grouped into a sedentary group (CLSed). [Figure 1] presents the flowchart for the experimental group formation.
Figure 1: Study flow chart. SL: Small litter group, CL: Control litter group, HIIT: High-intensity interval training.

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Maximum cardiorespiratory fitness tests (VO2 max) and training protocols

Immediately after weaning, the animals were subjected to a six-bay motorized treadmill (Insight®) adaptation period for 5 consecutive days, at 10-min periods and progressive speeds, where they were subsequently trained.

Before, during and after the training protocols, all animals, including those from the sedentary groups, were submitted to maximal aerobic capacity evaluations (VO2 max) on a metabolic treadmill (Panlab®) using a gas analyzer (Harvard Aparatus®). The protocol involved treadmill running to exhaustion at a 5° incline, starting at a speed of 6 m/min and increasing by 3 m/min every 3 min until the animals were unable to continue the exercise.[14] The applied tests aimed at assessing cardiorespiratory fitness, training efficiency and prescribing training loads in a more individualized manner, according to the cardiorespiratory capacity of each animal.

After forming the experimental groups, two physical training protocols were used: endurance and HIIT. The endurance protocol was characterized as a moderate intensity training (65%–70% VO2 max), lasting 60 min per session. Each training session consisted of a 10-min warm up (50% VO2 max) and 50 min of main exercise (65%–70% VO2 max). The training load adjustment was performed in the 4th week of training, after a new VO2 max evaluation. The HIIT sessions lasted 40 min, divided into a 10-min warm up (50% VO2 max) and six 3-min high-intensity running periods (85%–90% VO2 max), interspersed by 2 min of low intensity running (50% VO2 max), totaling 30 min for the main exercise. All training protocols began after the adaptation period and the first VO2 max. Training test was performed at around the 30th postnatal day, at a frequency of three weekly sessions every other day for 8 weeks.

Body weight, food intake, and organ weighing

The body weight of CL and SL animals was recorded weekly from the 4th postnatal day until the 90th day of life. Lee's index (LI) for the assessment of overweight/obesity was calculated as [LI = (BM × 1/3)/NAL × 100], where BM = body mass (g) and NAL = nasoanal length (cm). Food intake was also obtained weekly by the difference between the amount of offered food and the remaining food after 24 h.

The animals were euthanized 48 h after all in vivo procedures, by diaphragmatic rupture under anesthesia. The anesthetic protocol consisted in a combination of intraperitoneally applied dissociative anesthetic ketamine hydrochloride at 90 mg/kg. (Vetanarcol®, Konig, Brazil) and the sedative and myorelaxant xylazine hydrochloride, at 10 mg/kg (Kensol®, Konig, Brazil). Both drugs were mixed and applied. After total exsanguination by cardiac puncture under general anesthesia, the collected blood was centrifuged, and the serum stored at −80°C. Immediately after euthanasia, the retroperitoneal and perigonadal adipose tissues, left and right testicles, right epididymis, seminal vesicle, and prostate were removed and weighed using a precision balance (Bioprecisa®-0.0001 g- Brazil). Weight data were expressed as relative weight (%).

Oral glucose tolerance test, insulin tolerance test (ITT), and biochemical serum analysis

To perform both tests, the animals were fasted for 6 h. Blood was collected by lancing the animals' tail to measure capillary glucose, analyzed using an AccuChek Advanced glucometer (Roche®, Germany). The tests were performed during the week prior to euthanasia, at 72-h intervals.

Concerning the Oral Glucose Tolerance Test (OGTT), basal glucose (T0) was measured and subsequently a 2 g/kg body weight 50% glucose solution was administered through gavage. Subsequent blood samples were collected at T1 (15'), T2 (30'), T3 (60'), and T4 (120').

Regarding the ITT, the animals received an intraperitoneal insulin infusion (1 U/kg body weight) and blood samples were collected before (T0') insulin administration and subsequently at T1 (5'), T2 (15'), T3 (30'), and T4 (45'), after administration. The plasma glucose decay constant (kitt) was calculated as 0.693/(t1/2), where t1/2 is calculated from the slope of the lowest quadratic analysis of plasma glucose concentrations after insulin injection.[15]

Biochemical analyses were performed on a CobaS c111 automated device (Roche®) using CobaS c111 kits for the measurement of serum creatinine, total cholesterol, high-density lipoprotein, low-density lipoprotein, triglycerides, and glucose.

Sperm counts

Sperm were collected from the epididymal secretion through a small incision in the left epididymis tail. The secretions were placed in 50 μL of a phosphate buffered saline (PBS) buffer solution (Sigma®). After secretion homogenization with PBS, a 20 μL aliquot of this solution was removed and placed in 6 mL of distilled water for sperm immobilization (1:300 dilution). The diluted sample was used for sperm counts in a Neubauer chamber under an optical BH-2 light microscope (Olympus®, Japan) at 100 × magnification. The average sperm count of the four lateral quadrants on both sides of the chamber was considered to obtain sperm concentrations, calculated as:

Sperm concentrations (sptz/mL) = Obtained average × 300 × 104.

Sperm vitality assessment

Sperm smears were prepared and stained by the nigrosin-eosin technique,[16] where two hundred sperm from each animal were evaluated and classified as living or dead, under a BH-2 light microscope (Olympus®, Japan) light microscope, at 1.000 × magnification. Data were expressed as percentage of live sperm.

Sperm morphology evaluation

To determine the sperm abnormality index and morphological classification, sperm smears were prepared and stained by the Shorr technique,[16] where two hundred sperm from each animal were evaluated, classified as normal and abnormal under a BH-2 light microscope (Olympus®, Japan) light microscope, at 1.000 × magnification. Abnormalities were defined as head (amorphous) and tail defects (broken and coiled) according to Oshio et al.[17] and Seed et al.[18]

Histometric analyses

The right epididymis and right testis were used for this analysis. The epididymis was fixed in Bouin for 24 h. The testis was fixed in a modified Karnovsky fixative (4% paraformaldehyde: 4% glutaraldehyde in 0.1 mL/L PBS, pH 7.4). The organs were embedded in paraffin, sectioned at 5 μm thickness for Gomori trichrome staining in the epididymis and hematoxylin and eosin staining in the testes. The epididymis epithelium height was determined from four measurements per tubule in 10 transverse tubules/animal in the initial segment and epididymis caudal portion. The average height of the epithelium per tubule was calculated and six animals per group were analyzed. The height of the seminiferous tubule epithelium was determined by averaging four opposite measurements (basal lamina to the last nucleated cell), the luminal diameter was calculated by the difference between the total diameter and the sum of two horizontal epithelium heights. The most circular tubules possible from six testicles per group and 20 tubules per animal were analyzed. The histological sections were photographed under a light microscope model AXIOPHOT HBO50 (Zeiss®) coupled to an AXIOCAM ICc3 (Zeiss®) camera. The Image Pro Plus® Image Capture Program-Version 6 was used for measurements.

Statistical analyses

The Shapiro–Wilk test was performed to verify data normality. To verify possible changes in SL animals, comparisons were carried out between the CLSed and SLSed groups using Student's t-tests, while a one-way ANOVA followed by Tukey's post hoc were used for intergroup comparisons of SL animals. To obtain the OGTT results, the total area under the glycemic curve was calculated. Results are expressed as mean ± standard deviation and a significance level of P < 0.05 was adopted. All statistical analyses were performed using the SPSS (SPSS Inc.®, version 21) and GraphPad Prism® 5.0 (San Diego, CA, USA) softwares.


  Results Top


The body mass of SL animals before weaning was significantly higher from the 4th day of life when compared to CL animals, and this difference was maintained between the CLSed and SLSed groups after weaning during all evaluated periods [Figure 2]a and [Figure 2]b. However, no significant differences in body mass between the SLSed, SLEnd and SLHIIT groups after weaning until 90th day was observed [Figure 2]b.
Figure 2: Body mass, food intake, oral glucose tolerance test and insulin tolerance test of animals. Body mass of animals (a) before weaning. Body mass of animals (b) control litter sedentary, small litter sedentary, small litter endurance and small litter high-intensity interval training after weaning. Food intake of animals (c) control litter sedentary, small litter sedentary, small litter endurance and small litter high-intensity interval training after weaning. Oral glucose tolerance test (area under the curve) of animals (d). Insulin tolerance test (Kitt) of animals (e). Results presented in mean and standard deviation values. To all parameters, 10 rats were used for both groups. *Control litter and small litter intergroups differences; SL intergroups differences. abSame letters: Significant differences. P < 0.05.

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As shwon in [Figure 2]c, SLSed animals displayed significantly higher food intake in eight of nine measurements compared to CLSed animals. Regarding SLSed, SLEnd and SLHIIT food intake, significant differences were observed during the second evaluation week, with the SLSed group presenting a higher consumption average than the SLEnd and SLHIIT groups.

[Figure 2]d and e indicate the OGTT results of the CLSed, SLSed, SLEnd, and SLHIIT groups. The mean area under the curve of the SLSed animals was 11.2% statistically higher compared to the results of the CLSed animals. The OGTT results in SL animals indicate no statistically significant differences between the endurance and HIIT trained groups compared to the SLSed groups. Regarding the ITT, SLSed animals presented a significant 39% lower mean glucose decay constant (kitt) when compared to the CLSed group mean, demonstrating higher insulin resistance in the overfed group. Among the SL groups, the SLSed group presented lower glucose decay constant (kitt) values during ITT when compared to both the SLEnd group (51%) and the SLHIIT group (60%), demonstrating higher insulin resistance in sedentary overfed animals when compared to the trained endurance and HIIT groups.

[Table 1] presents the results of the CLSed, SLSed, SLEnd, and SLHIIT groups for body mass at 90 days of life, NAL, LI and adiposity (relative perigonadal and retroperitoneal adipose tissue weights). Regarding body mass, the SLSed group presented a significantly higher means when compared to the CLSed group. However, no differences for NAL and LI were observed. Adiposity, represented by the relative perigonadal and retroperitoneal adipose tissue weights, was significantly higher in the SLSed group when compared to the CLSed group, presenting 26% and 58% higher means, respectively.
Table 1: Comparison of the final body mass, lee index, nasoanal length and adiposity of the control litter sedentary, small litter sedentary, small litter endurance and small litter high-intensity interval training groups of animals

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Among the SL groups, no statistically significant differences in final body mass, NAL and LI were detected. However, significant differences were observed for adiposity. The SLSed group presented higher relative perigonadal adipose tissue weight means compared to the SLEnd (20%) and SLHIIT (19%) groups, as well as for retroperitoneal adipose tissue compared to the two trained groups, with differences of 38% (SLEnd) and 32% (SLHIIT), respectively.

Serological biochemistry comparisons between the CLSed and SLSed groups indicated a significant difference in serum glucose, with the SLSed group presenting a 14% higher means. In addition, despite the absence of statistical differences, the mean total cholesterol and triglycerides of the SLSed group were 10% and 38% higher when compared to the means of the CLSed groups, respectively [Table 2]. Among the SL groups, the SLSed group presented 12% and 15% higher mean serum glucose levels than the SLEnd and SLHIIT groups, respectively.
Table 2: Comparison of biochemical variables of the control litter sedentary, small litter sedentary, small litter endurance and small litter high-intensity interval training groups of animals

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Regarding reproductive parameters, no differences in sperm concentrations, vitality and morphology between the CLSed and SLSed groups and intergroups (SLSed, SLEnd and SLHIIT) were observed [Table 3]. However, SLSed animals showed relative epididymis reductions of 10.5%, seminal vesicle reductions of 16% and prostate reductions of 13% compared to CLSed animals, with no difference between SL groups [Table 4]. No significant changes regarding histometric seminiferous and epididymal tubule parameters between the SLSed and CLSed animals were observed, as well as between the SL groups [Table 4].
Table 3: Evaluation and comparison of sperm parameters of control litter sedentary, small litter sedentary, small litter endurance and small litter high-intensity interval training groups

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Table 4: Evaluation and comparison of reproductive organs weight, testicles and epididymis of the control litter sedentary, small litter sedentary, small litter endurance and small litter high-intensity interval training groups

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  Discussion Top


It is well established that stimuli at critical development stages, such as the postnatal period, can trigger long-term chronic disease development.[1] In the present study, the litter reduction protocol was used to induce lactation overfeeding and proven efficient in altering metabolic parameters in these animals. The animals belonging to the SLSed group displayed food intake alterations and increased central adiposity, as well as glycemic profile alterations in adulthood, even when fed standard food, similar to the results reported by Plagemann et al.,[19] Boullu-Ciocca et al.,[20] and Collden et al.[21] The SL animals submitted to exercise protocols after weaning (SLEnd and SLHIIT) displayed a significant difference only in one of the nine evaluated points concerning food intake in relation to the SLSed group. However, although no difference in final body mass was detected, a decrease in retroperitoneal and perigonadal fat in both exercised groups was observed when compared with SLSed animals, demonstrating the efficiency of the adopted protocols in decreasing visceral adiposity in trained SL animals. Andreazzi et al.[15] and Patterson et al.[22] reported that exercise started shortly after weaning considerably inhibited the onset of obesity induced by dietary treatment in rats or neonatal treatment with monosodium glutamate in mice, respectively, suggesting that early physical training may favorably alter the development of hypothalamic pathways that control energy homeostasis during brain development.

The negative effects of obesity on male reproductive parameters have been well reported in several studies.[23],[24] However, no studies in the literature relating the effects of overweight/obesity induced by infancy overfeeding on reproductive parameters and the effect of infancy-initiated physical activity on overfed Wistar rats are available. Despite negative metabolic changes and increased central adiposity, SLSed animals did not present altered sperm morphology, concentration and vitality compared to CLSed animals, suggesting that infancy overfeeding-induced obesity did not affect the evaluated sperm parameters. However, these animals displayed a reduction in seminal, epididymis and prostate bladder weight when compared to CLSed animals, in contrast to the results reported by Palmer et al.,[8] which may be due to the assessed species and obesity induction method.

Seminiferous tubules are the main testis constituent in most mammals, able to influence testicular weight and daily sperm production.[25] In studies involving the spermatogenic process, tubular diameter and height of the seminiferous epithelium are commonly used as spermatogenic activity indicators, as they contribute to the size and quantity of Sertoli and germ cells. Epididymis tubule epithelium height has been used in several studies as a method to investigate deleterious reproduction effects.[26]

In the present study, infancy overfeeding did not lead to changes in the spermatogenic process or effects on the epididymis epithelium. Yang et al.[27] reported changes in the seminiferous tubules of obese rats fed a high calorie diet. In that study, the seminiferous tubules were not well developed, and their cell layers organized atypically. This discrepancy is probably related to the obesity induction method and period.

The exercised groups in the present study showed no changes in the evaluated reproductive parameters, corroborating the study carried out by Takashiba et al.,[28] who evaluated the effects of a cafeteria diet and treadmill training on Wistar rat testis. The authors reported no observed diet and/or training alterations concerning testicular weight, tubular diameter and height of the seminiferous epithelium, and no differences in the histological organization of the seminiferous testes and tubules were noted. However, Palmer et al.[8] evaluated the reversibility of sperm changes associated to obesity induced by high fat diet in mice in response to weight loss through diet and exercise. Diet and/or exercise improved sperm motility and morphology, improved sperm DNA damage and sperm-oocyte binding, suggesting that diet and lifestyle interventions could be a combined approach to battle subfertility in overweight and obese individuals.

In humans, Håkonsen et al.[7] reported weight loss associated with increased total sperm count and normal morphology, plus increased testosterone and sex hormone binding protein in men who participated in a weight loss program based on diet and daily physical activity. These differences are associated with characteristics inherent to physical activities (duration, intensity, and type of modality) as well as individual characteristics, implying different changes in the metabolic and/or reproductive parameters of these individuals.

Although the changes caused by the litter reduction method for obesity induction did not affect the reproductive parameters of SL animals, the training protocols adopted in the study should be highlighted. The literature reports conflicting data regarding the practice of physical exercise and the effects on male reproductive parameters, especially on optimal intensity and volume.[10] Vaamonde et al.[29] demonstrated negative effects of increased training intensity on seminiferous parameters, mainly related to sperm morphology. Wise et al.[30] found that a volume >5 h per week was associated with lower sperm concentrations. Safarinejad et al.[31] described negative effects on sperm quality in men undergoing high intensity or high-volume protocols, which may indicate that these two variables, when poorly quantified, may be detrimental to male fertility.

Limitations in the present study comprise the scarcity of studies that applied the same obesity induction model, relating this to reproductive aspects, in addition to the influence of the two types of adopted physical training. However, a positive point of this study is that the intensity of the endurance and HIIT protocols developed from the VO2 max. for each animal, as well as the time and frequency of the adopted sessions and the early start of the training did not negatively influence the analyzed reproductive parameters and were confirmed as effective in improving metabolic changes caused by overfeeding during lactation. Thus, the development of new studies involving the effects of metabolic programming by overfeeding during lactation on reproductive parameters is proposed, as well as the evaluation of the possible effects of different types of physical exercise, volume, intensity, and types of exercise in this body weight gain induction model.


  Conclusion Top


Overfeeding during lactation leads to metabolic parameter alterations, but did not negatively influence male reproduction aspects. The endurance and HIIT protocols initiated in infancy in Wistar rats proved to be effective in reversing these metabolic changes without impairing the evaluated reproductive parameters, highlighting the benefits and safety of the two types of adopted exercise.

Acknowledgments

The authors would like to thank Centro de Biologia da Reprodução, Rede Mineira de Bioterismo and Rede Mineira Toxifar.

Financial support and sponsorship

Rede Mineira de Bioterismo–FAPEMIG (Project Number RED 00009/14). Rede Mineira Toxifar–FAPEMIG (Project Number RED 00008/14).

Conflicts of interest

There are no conflicts of interest.



 
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    Figures

  [Figure 1], [Figure 2]
 
 
    Tables

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



 

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