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tes have the risk of transmitting intestinal parasites in sports environments, leading to their poor performance. This study aimed to investigate iron deficiency, iron deficiency anemia, anaerobic performance, and muscle strength in athletes with intestinal parasites. It was conducted by

defi- ciency, weakness, muscle weakness during the infec- tion, and dysregulation of the gastrointestinal system need to be relieved. ABSTRACT Athletes have the risk of transmitting intestinal parasites in sports environments, leading to their poor performance. This study aimed to investigate iron deficiency, iron deficiency anemia, anaerobic performance, and muscle strength in athletes with intestinal parasites. It was conducted by the Ministry of Youth and Sports, General Directorate of Sports Services, Department of Health Affairs in 2018. The stool test results of the athletes were examined. The iron deficiency, iron deficiency anemia, an- aerobic performance, and muscle strength were determined by stool sample analysis (study group) and compared with those of 28 athletes who performed the same sports and had no parasites (control group). The iron deficiency and iron deficiency anemia in all athletes were evaluated using iron and ferritin levels in blood analysis. The anaerobic performance was assessed using the Wingate test. The isokinetic muscle strength was evaluated using the IsoMed 2000 isokinetic dynamometer. No statistically significant difference in blood analysis and iron and ferritin levels was found between the groups. No athlete had iron deficiency or iron deficiency anemia. On comparing the anaerobic performances of the groups, no statistically significant difference in WanT parameters was observed. A statistically significant difference was found in the strength of the dominant leg knee extensor muscles at an angular velocity of 60º/s, but no statistically significant differences were noted in other muscle strength parameters. Asymptomatic intestinal parasites did not lead to iron deficiency or iron deficiency anemia and did not affect anaerobic performance in athletes, but adversely affected the strength of dominant leg knee extensor muscles. Key words: Anemia, infection, isokinetic, sport, Wingate test Original Article Parasitology 1 Ministry of Youth and Sports, Sports General Directorship, Department of Health Services, Center of Athlete Training and Health Research, Ankara, Turkey 2 Department of Physiotherapy and Rehabilitation, Faculty of Health Sciences, Ankara Yıldırım Beyazıt University, Ankara, Turkey Effect of intestinal parasites on anaerobic performance and muscle strength in athletes Tuğba Kocahan 1 , Bihter Akınoğlu 2 , Adnan hasanoğlu 1 17 Medical Journal of

Sports, Sports General Directorship, Department of Health Services, Center of Athlete Training and Health Research, Ankara, Turkey 2 Department of Physiotherapy and Rehabilitation, Faculty of Health Sciences, Ankara Yıldırım Beyazıt University, Ankara, Turkey Effect of intestinal parasites on anaerobic performance and muscle strength in athletes Tuğba Kocahan 1 , Bihter Akınoğlu 2 , Adnan hasanoğlu 1 17 Medical Journal of Islamic World Academy of Sciences doi: 10.5505/ias.2019.89847 2019;27(1): 17-24 Introduction

Medical Journal of Islamic World Academy of Sciences 2019; 27(1):17-24 18Kocahan, AkğnoŞlu, HasanoŞlu Athletes are at risk of intestinal parasitic infec- tions due to poor environmental conditions in sports settings. Public areas, such as preparatory camps, na- tional team camps, and/or boarding camp training centers, besides frequent travel, expose athletes to poor hygiene conditions in terms of food and envi- ronment (10). At the same time, the immune system is frequently suppressed in athletes who perform long-term and severe exercises (11). Thus, after se- vere exercise, athletes become more susceptible to microorganisms, especially viral infections. After heavy exercise, viruses and bacteria can enter the body to increase the risk of subclinical and clinical infections (12). These conditions may lead to poor performance (13-15). Intestinal parasites may cause anemia in ath- letes and adversely affect sports performance (16, 17). The hemoglobin concentration is low in anemia. The most common cause is iron deficiency. Iron is an important mineral for optimal athletic performance due to its role in energy metabolism, transport of oxygen, and acid–base balance. It promotes athletic performance by increasing oxygen-carrying capacity (30). The reduced iron tank adversely affects aerobic capacity, muscle strength, and endurance (16, 17). The gastrointestinal tract is an important part of the immune system and nutrition. A well-balanced gastrointestinal tract, adequate and balanced nutri- tion of the athlete, bioavailability of the food, and optimization of the immune system are important for promoting sports performance. Hence, it is hy- pothesized that anaerobic performance and muscle strength are adversely affected in the elite athletes with intestinal parasites due to the effects of para- sites on the gastrointestinal system and deterioration of nutrition. Therefore, this study aimed to determine the presence of iron deficiency anemia or iron defi- ciency in athletes with intestinal parasites and exam- ine the muscle strength and anaerobic performance. MATERIALS AND METHODS This study was conducted by the Ministry of Youth and Sports, General Directorate of Sports Ser- vices, Department of Health Affairs in 2018. The stool test results of the athletes applying for health and performance evaluation were examined. The study was performed with

in athletes with intestinal parasites and exam- ine the muscle strength and anaerobic performance. MATERIALS AND METHODS This study was conducted by the Ministry of Youth and Sports, General Directorate of Sports Ser- vices, Department of Health Affairs in 2018. The stool test results of the athletes applying for health and performance evaluation were examined. The study was performed with a total of 56 athletes: 28 athletes who had parasites detected in the stool sample anal- ysis and had no other disease (study group) and 28 athletes who did not have any parasites and did not have any known diseases (control group). The study group and the control group athletes were demo- graphically similar (Table 1). The permission and approval of the Ministry of Youth and Sports, General Directorate of Sports Ser- vices, Department of Health Affairs (dated 28.12.2018 and numbered 39746592-100-E.809306) were ob- tained to perform the study and use the data of the athletes who met the research criteria. The first-day blood tests and stool tests were performed for all athletes participating in the study. The athletes were administered the anaerobic capac- ity test on the same day, and the isokinetic muscle strength test was conducted the next day. All ath- letes were informed before the tests and asked to put on sportswear and sports shoes. Study group (n = 28) Control group (n = 28) P Age (year) 17.25 ± 1.69 17.07 ± 1.53 0.681 * Height (cm) 174.55 ± 9.70 174.68 ± 9.18 0.997 * Weight (kg) 68.35 ± 13.27 68.72 ± 14.34 0.921 * BMI (kg/m 2 ) 22.39 ± 3.04 22.51 ± 3.28 0.894 * Sports age (year) 5 (3–11) 5.50 (3–9) 0.959 ** Gender, n (%) Male 20 (72) 20 (72) Female 8 (28) 8 (28) Table 1: Descriptive characteristics of the groups BMI, Body mass index. *Independent-samples t test. **Mann–Whitney U test.

Medical Journal of Islamic World Academy of Sciences 2019; 27(1):17-24 19Eğect of intestinal parasites on anaerobic performance and muscle strength in athletes Blood analysis The fasting blood sample was taken from the an- tecubital vein of the athletes on the first day. It was collected in two tubes [one containing EDTA, and the other containing a clot activator (SST II Advance)]. Red blood cell (RBC) count, hemoglobin (HGB), hematocrit (HCT), mean corpuscular volume (MCV), mean corpuscular hemoglobin (MCH), red cell distri- bution width (RDW), white blood cell (WBC) count were measured using the Sysmex CBC XT2000I coun- ter (Sysmex Corporation, Kobe, Japan). Impedance was used for RBC count, photometric analysis for HGB, cumulative impedance for HCT, and fluores- cence flow cytometry for WBC count. The MCV and MCH values were calculated using the RBC count and HCT. Randox RX Imola (UK) clinical chemistry device was used to measure iron (Fe) and ferritin values. Spectrophotometry was used for iron (Fe), and turbi- dimetry methods were used for ferritin value. Stool sample analysis Before the analysis, the athletes were given spe- cial closed plastic containers for stool collection, and the stool samples were studied within 1 h. The stool samples were first examined macroscopically. Then, two samples were prepared with 22 x 22 lamellae us- ing saline solution with the Olympus CX23LEDRFS1 model light microscope having zigzag scanning with 10x lens and then one-third of the lamella with 40x lens. The same biologist examined all the materials. The type of parasite was determined in the 40x lens examination. Evaluation of anaerobic capacity The Wingate test (WanT) was used to evaluate the anaerobic capacity of the athletes. WanT is a test to measure the explosive force, which is continuity in strength and muscular fatigue, to obtain information about muscle metabolism in short-term and high-in- tensity exercises, and also to evaluate athletic perfor- mance. The Monark 891E model leg bicycle ergom- eter, which was connected to the modified computer for WanT and worked with compatible software, was used. The saddle and pedal length settings were made for each athlete before the test. In the

fatigue, to obtain information about muscle metabolism in short-term and high-in- tensity exercises, and also to evaluate athletic perfor- mance. The Monark 891E model leg bicycle ergom- eter, which was connected to the modified computer for WanT and worked with compatible software, was used. The saddle and pedal length settings were made for each athlete before the test. In the lower- extremity WanT, the load equivalent to 7.5% of body weight was calculated automatically on the comput- er and placed on the scale. Before starting WanT, the athletes cycled the bike for about 3 min with 60–80 pedal speed (rpm). In the last 5 s of every 1 min, a high-speed load of 120–160 rpm was applied. After completing the warm-up, the athletes performed a 2-min stretch, following which they were allowed to cool down. When the athlete was ready, the test was started and the driver was asked to pedal for 30 s. The number of pedals and load at the end of 30 s was calculated, and total work = anaerobic capacity (in Joule) was determined. With the mathematical mean of the total work, the average job = anaerobic power was calculated (in Watt). During WanT, the highest power value during any 5 s (initial seconds) was re- corded as the peak power, which was an indicator of the anaerobic energy capacity. The minimum power value in 5 s (last seconds) was recorded as the mini- mum power. The fatigue index was calculated by us- ing the following formula: (peak power – minimum power/peak power) x 100. After completing the test, the athlete was allowed low-speed cooling for 3 min, and the test was terminated (18). Evaluation of isokinetic muscle strength The isokinetic muscle strength of the knee flex- or and extensor muscles was evaluated using the IsoMed 2000 device. The athletes underwent a warm- up run for 10 min before the test. After the warm-up, they were taken to the isokinetic device, and the de- vice was adjusted according to the individual anthro- pometric structure of the athletes. During the test, the body weight and age values

flex- or and extensor muscles was evaluated using the IsoMed 2000 device. The athletes underwent a warm- up run for 10 min before the test. After the warm-up, they were taken to the isokinetic device, and the de- vice was adjusted according to the individual anthro- pometric structure of the athletes. During the test, the body weight and age values were entered into the computer and the program was installed. The suitability of the movement width of the joint and the angles to be tested was determined by making a sample movement at very low speed to the athletes. The effect of gravity was reset. Evaluations were done in the sitting position, taking into account the range of motion of the athletes and the measurement char- acteristics of the device. Accordingly, the knee flex- ion/extension movement was performed between 90° and 0° flexion angles in the sitting position while the trunk was at 70° flexion. The evaluation protocol was created in two stages for each angular velocity. In the first stage, the athletes were asked to perform three repetitive submaximal movements at 60°/s for familiarization to the movement and for warm- ing up. In the second stage, the test was completed by making a maximum of five repetitive motions

Medical Journal of Islamic World Academy of Sciences 2019; 27(1):17-24 20Kocahan, AkğnoŞlu, HasanoŞlu at 60°/s angular velocity. Similarly, the athletes were asked to perform three repetitive submaximal move- ments at 180°/s for familiarization to the new angular velocity and for warming up. In the second stage, the test was completed by making maximal 15 repetitive motions at 180°/s angular velocity. Between maximal movements, one minimum rest break was given. Peak torque (PT) and PT/kg values of the athletes at both an- gular speeds were recorded. Measurements were taken bilaterally, first on the dominant side and then on the nondominant side. The athletes were encouraged to perform maximal performance with verbal commands. All tests were performed by the same physiotherapist who worked for at least 3 years in this area (19). Statistical analysis All the data obtained from the groups were ana- lyzed using the Statistical Package for Social Sciences Inc. (SPSS, IL, USA) for Windows Release 20.0 statisti- cal package program. The variables determined by measurement were expressed as mean ± standard deviation (X ± SD), and the percentage (%) value was calculated for the variables by counting. For compar- ing two groups in terms of numerical variables, the independent-samples t test was used for parametric data and the Mann–Whitney U test was used for non- parametric data. In all statistics, a P value less than 0.05 indicated statistical significance. RESULTS The age, height, weight, body mass index, sports age, and gender distribution of the study and control groups were similar (P < 0.05) (Table 1). In the study group, the distribution of parasites was determined as Ascaris lumbricoides in eight cas- es (28.6%), Taenia saginata in eight cases (28.6%), E. histolytica in seven cases (25%), Entamoeba coli in three cases (10.7%), and Giardia intestinalis in two cases (7.1%) (Table 2). No statistically significant difference in blood analysis and iron and ferritin levels was found be- tween the groups (P > 0.05), and no athlete had iron deficiency or iron deficiency anemia (Table 3). When the anaerobic performances of the groups were compared, no statistically significant difference was observed in

cases (10.7%), and Giardia intestinalis in two cases (7.1%) (Table 2). No statistically significant difference in blood analysis and iron and ferritin levels was found be- tween the groups (P > 0.05), and no athlete had iron deficiency or iron deficiency anemia (Table 3). When the anaerobic performances of the groups were compared, no statistically significant difference was observed in total work, average work, peak pow- er, minimum power, and fatigue index between the groups (P > 0.05) (Table 4). When the isokinetic muscle strength values of the groups were compared, the strength of the domi- nant leg knee extensor muscles was found to be less in the study group at the angular velocity of 60º/s (P < 0.05). No statistically significant difference was observed in the other muscle strength parameters evaluated at angular velocities of 60º/s and 180º/s (P > 0.05) (Table 5). DISCUSSION This study examined iron deficiency anemia, anaerobic performance, and muscle strength in ath- letes with intestinal parasites who were asymptom- atic without any clinical complaints. It was found that iron deficiency or iron deficiency anemia did not develop in athletes with intestinal parasites and an- aerobic performance was not affected. The explosive muscle strength of the dominant leg knee extensor muscle was found to be less in the study group with intestinal parasites. Intestinal parasitic infections are one of the most common infections worldwide. A. lumbricoides, Trichuris trichiura, and hookworm are the most com- mon intestinal parasites from soil-borne helminths (20). Giardia lamblia, which causes giardiasis, is the most common intestinal protozoan in developed and developing countries (21). Another common bowel protozoan is E. histolytica, which frequently causes chronic bowel infection (22). In Turkey, vari- ous studies were conducted to investigate the dis- tribution of parasites by age groups. G. intestinalis with Enterobius vermicularis was reported in the 0–14 age group. Blastocystis hominis and G. intesti- nalis were more frequently found in adulthood and childhood, respectively (2). A retrospective study ex- amining the prevalence of intestinal parasites in the Detected intestinal parasitesTotal number % Ascaris lumbricoides 8 28.6 Taenia saginata 8 28.6 Entamoeba histolytica 7

parasites by age groups. G. intestinalis with Enterobius vermicularis was reported in the 0–14 age group. Blastocystis hominis and G. intesti- nalis were more frequently found in adulthood and childhood, respectively (2). A retrospective study ex- amining the prevalence of intestinal parasites in the Detected intestinal parasitesTotal number % Ascaris lumbricoides 8 28.6 Taenia saginata 8 28.6 Entamoeba histolytica 7 25 Entamoeba coli 3 10.7 Giardia intestinalis 2 7.1 Table 2: Proportional distribution of intestinal parasites dete- cted in the study group

Medical Journal of Islamic World Academy of Sciences 2019; 27(1):17-24 21Eğect of intestinal parasites on anaerobic performance and muscle strength in athletes Blood parameters Study group (n = 28) Control group (n = 28) P * RBC (×10 6 /µL) 5.22 ± 0.44 5.32 ± 0.45 0.434 Hemoglobin (g/dL) 15.35 ± 1.25 15.35 ± 1.25 0.684 Hematocrit (%) 43.39 ± 3.94 43.84 ± 3.54 0.652 MCV (fL) 83.02 ± 3.39 82.53 ± 3.87 0.617 MCH (pg) 29.03 ± 1.49 28.92 ± 1.43 0.771 RDW (%) 12.34 ± 0.51 12.44 ± 0.70 0.556 WBC (×10 3 /µL) 7.35 ± 2.65 7.11 ± 2.40 0.730 Iron (µg/dL) 87.39 ± 39.50 83.85 ± 31.49 0.713 Ferritin (ng/mL) 49.00 ± 23.82 54.90 ± 26.44 0.385 Table 3: Blood test results of the groups MCH, Mean corpuscular hemoglobin; MCV, mean corpuscular volume; RBC, red blood cell; RDW, red cell distribution width; WBC, white blood cell. *Independent-samples t test. Wingate test parameters Study group (n = 28) Control group (n = 28) P * PP (W) 878.91 ± 267.80 822.27 ± 245.70 0.413 PP (W/kg) 12.52 ± 2.60 12.13 ± 2.74 0.584 tPP (ms) 1582.29 ± 742.09 1821.29 ± 914.64 0.288 AP (W) 583.25 ± 169.52 555.88 ± 150.63 0.526 AP (W/kg) 8.30 ± 1.48 8.21 ± 1.61 0.837 MP (W) 296.07 ± 144.82 299.46 ± 117.21 0.924 MP (W/kg) 4.25 ± 1.90 4.41 ± 1.54 0.724 PD (W) 582.84 ± 231.71 522.81 ± 207.57 0.312 PD (W/kg) 8.28 ± 2.80 7.71 ± 2.82 0.453 PD (W/s) 19.86 ± 8.31 17.61 ± 7.34 0.288 PD [W/(s/kg)] 0.29 ± 0.11 0.26 ± 0.12 0.412 PD (%) 65.56 ± 15.38 62.41 ± 12.90 0.410 Table 4: Wingate test results of the groups *Independent-samples t test. province of Istanbul found the prevalence to be 5% (5486/111,889). The most commonly detected four parasites were as follows: G. intestinalis (62%), E. ver- micularis (16%), A. lumbricoides (7%), and B. hominis (6%) (6). Similarly, in a retrospective study in Sivas province, the prevalence of intestinal parasites was found to be 10.5% (532/5057). The most common parasites were G. intestinalis (3.7%), E. histolytica/