Abstract

693

Revista MVZ Córdoba

Rev. MVZ Córdoba

0122-0268 1909-0544

Universidad de Córdoba

Colombia revistamvz@gmail.com

69357845014

https://doi.org/10.21897/rmvz.1523

Original

Effects of L-carnitine supplementation on ascites syndrome in the broilers grown at high altitude

Efectos de la suplementación con L-carnitina en el síndrome de ascitis en los pollos de engorde criados a gran altura

İkbal Coşkun

Muhammed

Muhammedikbalcoskun@gmail.com Tekeli

Ahmet

atekeli@ogu.edu.tr

Van Yuzuncu Yıl University, Deparment of Animal Science, Van, Turkey Van Yuzuncu Yıl University Turquía Eskişehir Osmangazi University, Deparment of Animal Science, Eskişehir, Turkey Eskişehir Osmangazi University Turquía

January-May 2019

24 1 7127 7136 07 05 2018 08 10 2018 04 02 2019 https://creativecommons.org/licenses/by-nc-sa/4.0/

Esta obra está bajo una Licencia Creative Commons Atribución-NoComercial-CompartirIgual 4.0 Internacional.

Abstract

Objective. Investigate the effects of L-carnitine as a potential means of reducing the incidence of ascites in broilers and its relationship with physiological and biochemical paramaters. Material and methods. One-day-old 300 male broiler chicks (Ross 308) were used in the trial. The group without L-carnitine supplementation (0) was assigned as control and the groups that received 100, 150, 200 and 250 mg/L L-carnitine supplementation in water were assigned as treatment groups. The trial was completed in 35 days. Results. L-carnitine supplementation did not have any significant effect on live weight gain, feed consumption, water consumption and feed conversion ratio. Levels of blood plasma and hemogram parameters HDL, Triglyceride, CK, RBC and MCH were significantly affected by L-carnitine (p<0.05). Blood gas parameter pH value was significantly affected by L-carnitine supplementation in the broilers with ascites. Blood gas pH value significantly increased with 100 mg/L L-carnitine supplementation compared to that of control (p<0.05). While blood pH was 7.21 in the animals with ascites, it was determined as 7.48 in healthy animals. Concentrations of SO₂ and ctO₂ were higher in healthy animals, while ctCO2P and hemoglobin concentrations were higher in ascitic animals (p<0.05). Conclusions. Ascites mortality rates starting from the control group were calculated respectively as %; 20.00, 18.33, 26.67, 28.33 and 28.33%. 76.71% of total ascites deaths were in the 5th week. It was concluded that low doses of L-carnitine supplementation may have positive effects in the broilers grown at high altitude.

Resumen

Objetivo. Investigar los efectos de la L-carnitina como un medio potencial para reducir la incidencia de ascitis en pollos de engorde y su relación con parámetros fisiológicos y bioquímicos. Material y métodos. Se utilizaron 300 pollos de engorde machos de un día de edad (Ross 308) en el ensayo. El grupo sin suplementación de L-carnitina (0) se asignó como control y los grupos que recibieron suplementos de 100, 150, 200 y 250 mg/L de L-carnitina en agua se asignaron como grupos de tratamiento. La prueba se completó en 35 días. Resultados. La suplementación de L-carnitina no tuvo ningún efecto significativo sobre el aumento de peso vivo, consumo de alimento, consumo de agua y tasa de conversión alimenticia. Los niveles de plasma sanguíneo y los parámetros del hemograma HDL, triglicéridos, CK RBC y MCH se vieron afectados significativamente por L-carnitina (p<0.05). El valor del pH del parámetro del gas en sangre se vio significativamente afectado por la suplementación con L-carnitina en los pollos de engorde con ascitis. El valor del pH del gas en la sangre aumentó significativamente con la suplementación de 100 mg/L de L-carnitina en comparación con la del control (p<0.05). Mientras que el pH de la sangre fue de 7.21 en los animales con ascitis, se determinó como 7.48 en animales sanos. Las concentraciones de SO₂ y ctO₂fueron mayores en animales sanos, mientras que las concentraciones de ctCO2P y hemoglobina fueron mayores en animales ascíticos (p<0.05). Conclusiones. Las tasas de mortalidad por ascitis a partir del grupo control se calcularon respectivamente como %; 20.00, 18.33, 26.67 y 28.33. 76.71% de las muertes totales de ascitis fueron en la quinta semana. Se concluyó que dosis bajas de suplementos de L-carnitina pueden tener efectos positivos en los pollos de engorde criados a gran altitude.

Keywords Blood gas broiler L-carnitine performance parameters pulmonary hypertension

Palabras clave L-carnitina gas en sangre hipertensión pulmonar parámertos de rendimento pollos de engorde

<bold>INTRODUCTION</bold>

Carnitine is chemically in D- and L-form and only L-form exists in nature and is important for human and animal nutrition (1). L-carnitine is a white, highly water-soluble powder characterized by high thermal stability (up to 200 °C). Its chemical name is β-hydroxy-ϒ -trimethyl-amino butyrate. L-carnitine is also referred to as Vitamin BT (2). L carnitine has an important effect on energy production and fat metabolism in the body by providing mitochondrial transport of long chain fatty acids and mitochondria removal of short and medium chain fatty acids (3). In addition to its use in animal feeding (4), L-carnitine has also found use in a number of health sectors such as prevention of heart attacks and other heart conditions (5), hemodialysis (6) and infertility treatment (7).

Ascites (pulmonary hypertension) is a multifactorial syndrome resulted from interactions among genetic, environmental, dietary and physiological factors (8). Ascites is a cardiovascular disorder predominantly observed in fast-growing chickens rather than in chicks. In fast-growing chickens, hypobaric hypoxia (lack of oxygen) causes right ventricular hypertrophy (abnormal enlargement) and expansion. As a result, fluid accumulates in the abdominal region death causes due to oxygen deficiency (9). There are two hypotheses regarding the syndrome of ascites: Hypothesis 1: In the development of ascites syndrome, primary lesions occur in the lungs (pulmonary hypertension) and consequently the heart is affected (right ventricular hypertrophy). Hypothesis 2: Primary lesion in the development of ascites syndrome is caused by systemic hypertension-induced left ventricular insufficiency leading to right ventricular hypertrophy and acidosis (10). The prevalence of ascites has been reported to increase in the recent years. Selections made to achieve faster growth in chicks have improved genetic potential, but also caused some anatomical and physiological limitations and the same improvement led to negative impacts on the health of animals. A possible deterioration in oxygen resources (altitude, ventilation) will stimulate the development of many mechanisms in the cardiopulmonary system, which will trigger ascites syndrome.

L-carnitine supplementation is considered to relate to ascites syndrome due to its effect on energy metabolism. This study aimed to investigate the effects of L-carnitine as a potential means of reducing the incidence of ascites in broilers triggered by high altitude and its relationship with physiological and biochemical paramaters.

<bold>MATERIAL AND METHODS</bold>

Animal, feeds and feeding. One-day-old 300 male broiler chicks (Ross 308) with the same body weight average were used in the trial. At the trial, animals were separated into 5 groups each of which were divided into 3 subgroups. The group without L-carnitine supplementation was the control, and the groups supplemented with 100, 150, 200 and 250 mg/l L-carnitine in drinking water were the treatment groups. L-carnitine was used in its white, pure powder form and was obtained from Vimar Food Agriculture and Livestock Industry Trade Inc. / Turkey. L-carnitine was added to the drinking water on a daily basis. The trial was carried out in November 2014 and January 2015 at altitude of 1727 meters in Van-Turkey.

Ingredients and nutrient analysis results of the feeds used in the trial are given in table 1. Broiler chicks were fed with starter feed for days 1-10, followed by grower feed for days 10-21, and finisher feed for days 21-35. A corn-soybean meal basal diet was formulated according to NRC (1994). The broilers received pellet feeds throughout the whole period. Feed and water were given freely to all groups. The trial lasted 35 days. A 24-hour lighting program was applied throughout the trial.

Table 1 <bold>Table 1</bold>. Composition (g/kg) and nutrient contents (%) of mixed feeds used in the trial. Table 1 Table 1. Composition (g/kg) and nutrient contents (%) of mixed feeds used in the trial.

Ingredients Broiler starter diet (Days 1-10) Broiler grower diet (Days 10-21) Broiler finisher diet (Days 21-35)

Corn 411.07 450.70 460.74

Soybean meal (%46HP) 197.90 120.31 119.71

Full-fat soybean 140.00 160.00 160.00

Corn gluten flour (%60HP) 86.75 64.26 20.00

Rice (Broken) 40.00 40.00 40.00

Fish Flour (%53-60) 40.00 40.00 60.00

Sunflower meal (%36) 30.00 40.00 40.00

DCP (%18 P) 10.44 5.73 2.69

Chicken feather flour 10.00 10.00 10.00

Meat-bone flour (%35HP) 10.00 28.38 30.00

Corn extract (Full-fat) - 20.00 20.00

Soybean oil - - 19.45

Marble powder 9.43 6.83 5.73

L-Lysine 4.12 4.20 2.99

Sodium bicarbonate 3.20 2.65 1.82

DL-methionine 2.21 2.09 2.01

Salt 1.40 1.21 1.60

Vitamin premixture1 1.00 1.00 1.00

Mineral premixture2 1.00 1.00 1.00

L-Threonine 0.88 1.04 0.66

Anticoccidial 0.60 0.60 0.60

Total 1000.00 1000.00 1000.00

Analysed nutrients (%)

Dry matter 89.44 89.19 89.26

Crude protein 25.70 23.74 20.95

Crude Fat 4.42 5.12 7.65

Crude cellulose 3.11 2.48 3.11

Crude cinder 5.81 5.45 5.07

Calculated nutrients (%)

ME (kcal/kg) 3020 3120 3220

Lysine 1.44 1.34 1.21

Methionine 0.68 0.64 0.57

Calcium 1.05 0.95 0.85

Phosphorus 0.81 0.74 0.70

Sodium 0.18 0.17 0.16

¹: Per 1 kg diet: 12.500.000 IU Vitamin A, 3.500.000 IU Vitamin D3, 100.000 mg Vitamin E, 4.000 mg Vitamin K3, 3.000 mg Vitamin B1, 8.000 mg Vitamin B2, 5.000 mg Vitamin B6, 20 mg Vitamin B12, 70.000 mg Niacin, 20.000 mg Pantothenic Acid, 2.000 mg Folic Acid, 250 mg Biotin, 100.000 mg Vitamin C, 125.000 mg Antioxidant. ²: Per 1 kg diet: 120.00 mg Manganese, 40.000 mg Iron, 110.00 mg Zinc, 16.00 mg Copper, 500 mg Cobalt, 1.250 mg Iodine, 300 mg Selenium.

Blood biochemistry, mineral, hormone and blood gas values. For blood biochemical analyzes, blood samples were collected during the slaughter of 6 animals from each subgroup. Thirty minutes after collection of the blood samples, serums separated by centrifugation for 5 minutes at 4000 rpm were stored in ependorfs at -20°C until analysis. Blood biochemical analysis was performed by Swelab Alfa (Sweden) brand complete blood count device in whole blood samples. All samples were analyzed in a single study in one day. T3 and T4 hormones were detected in the plasma with Roche Diagnostic (United States) Elecsys e-411 Hormone Autoanalyzer using Roche Brand Kits. On the 35^th day of trial, blood samples taken from the wing veins of 3 ascitic and 3 healthy broilers from each subgroup were collected in heparin containing syringes to avoid clot formation. Blood gas, oximetry, electrolyte and metabolite parameters were measured by Radiometer ABL-700 Blood Gas Analyser.

Statistics. Variance analysis was employed based on General Linear Model (PROC GLM) procedure in accordance with the trial design (random parcels experimental design) and Duncan’s Multiple-Range Test was used to compare group averages. Statistical analyses were performed by SAS (version 9.2) statistical package software.

<bold>RESULTS</bold>

Performance parameters. Live weights of the treatment groups on weekly basis are given in table 2. When the groups were compared in terms of live weight gains, the differences between the group averages only at 7^th, 14^th and 28^th days were found to be statistically significant (p<0.05). By 35^th days, the end of trial, no significant differences were recorded between groups with respect to live weight (p>0.05).

Table 2 <bold>Table 2.</bold> The effects of L-carnitine supplementation in water on performance parameters and water consumption values (ml) of broilers. Table 2 Table 2. The effects of L-carnitine supplementation in water on performance parameters and water consumption values (ml) of broilers.

Days Treatment groups

Control 100mg/L L-carnitine 150mg/L L- carnitine 200mg/L L-carnitine 250mg/L L-carnitine SEM p=

Live Weight, g

Day 0 46.61 46.53 46.34 46.63 46.59 0.235 0.995

Day 7 207.63^ab 210.84^a 209.93^a 200.51^b 213.95^a 1.396 0.005

Day 14 568.00^a 532.22^b 558.63^a 519.54^b 575.78^a 3.443 0.001

Day 21 1095.84 1088.81 1087.84 1065.59 1090.39 7.033 0.699

Day 28 1809.95^a 1808.51^a 1699.46^b 1737.04^ab 1715.75^ab 14.975 0.042

Day 35 2475.56 2484.30 2486.94 2456.42 2386.84 23.470 0.689

Feed consumption, g

Day 7 211.25 213.05 211.15 206.75 211.93 1.027 0.239

Day 14 458.82 510.28 478.78 465.85 497.79 9.417 0.256

Day 21 789.93 785.33 753.93 803.07 797.24 11.357 0.525

Day 28 1045.90 1050.59 968.00 999.40 961.50 16.481 0.179

Day 35 1181.19 1184.35 1151.04 1140.43 1240.48 36.835 0.847

Total 3687.08 3743.59 3562.95 3615.49 3708.93 44.302 0.541

Feed efficiency ratio, kg feed consumption/kg live weight gain

Day 7 1.31 1.31 1.29 1.35 1.27 0.019 0.577

Day 14 1.27 1.59 1.37 1.47 1.38 0.041 0.116

Day 21 1.51 1.41 1.41 1.46 1.54 0.031 0.392

Day 28 1.45 1.45 1.48 1.51 1.48 0.040 0.978

Day 35 1.60 1.67 1.49 1.38 1.58 0.068 0.525

Water consumption (ml)

Day 7 390.33 381.33 377.33 372.10 377.67 5.388 0.754

Day 14 1050.33 1074.67 1006.33 1018.33 1036.67 25.279 0.845

Day 21 1703.27 1847.93 1736.27 1715.47 1638.03 58.234 0.762

Day 28 2751.00 2915.00 2844.63 2601.70 2500.20 87.828 0.393

Day 35 3571.07 3940.40 3721.73 3248.40 3150.87 113.085 0.107

Total 9465.67 10159.33 9686.37 8956.03 8703.43 265.058 0.292

*: Differences between group averages denoted by different letters in the same row are statistically significant (p<0.05). SEM: Standard error of difference between means.

L-carnitine supplementation in water did not have any significant effects on cumulative feed consumption of broilers by weeks and at the end of the trial (p>0.05). However, at the end of the trial, the highest amount of feed consumption was observed in the group receiving 100 mg/l L-carnitine, while the lowest was observed in the group receiving 150 mg/l L-carnitine.

As seen in table 2, no significant differences were detected in feed conversion ratios between groups throughout the trial (p>0.05). However, in the group receiving 200 mg/l L-carnitine supplementation, the feed efficiency ratio improved (1.38) numerically.

As indicated by table 2, no significant differences were recorded in water consumption values between groups throughout the trial (p>0.05). On the other hand, though not statistically significant, total water intake was higher in the group supplemented with 100 mg/ l L-carnitine compared to the other groups by the end of the trial.

Mortality rates. The effects of L-carnitine supplementation on mortality rates of broilers are presented in table 3. The lowest mortality rate (18.33%) was recorded in the group supplemented with 100 mg/l L-carnitine while the highest mortality rate (28.33%) was recorded in the groups supplemented with 200 and 250 mg/l L-carnitine.

Table 3 <bold>Table 3.</bold> The effects of L-carnitine supplementation on ascites mortality rates in broilers. Table 3 Table 3. The effects of L-carnitine supplementation on ascites mortality rates in broilers.

Treatment groups Number of deaths from sscites Mortality rate (%)

Control group 12 20.00

100 mg/l L-carnitine 150 mg/l L-carnitine 11 16 18.33 26.67

200 mg/l L-carnitine 250 mg/l L-carnitine 17 17 28.3328.33

Blood plasma and hemogram parameters. The effects of L-carnitine supplementation in water on selected blood plasma and hemogram parameters are shown in table 4. By the end of the trial, L-carnitine supplementation did not result in any significant differences between groups in blood plasma parameters Aspartate aminotransferase (AST), Alanine aminotransferase (ALT), Alkaline phosphatase (ALP), total protein, cholesterol, Low density lipoproteins (LDL), Triiodothyronine (T3) concentration and hemogram parameters Mean corpuscular volume (MCV), Red cell distribution width (RDW), Red cell distribution with actually (RDWa), hematocrit, platelet, hemoglobin concentrations (p>0.05). On the other hand, significant differences were recorded in High density lipoproteins (HDL), triglyceride, creatine kinase, glucose, Thyroxine (T4), Red blood cell count (RBC), Mean corpuscular hemoglobin (MCH) and Mean corpuscular hemoglobin concentration (MCHc) values between groups (p<0.05).

Table 4 <bold>Table 4.</bold> The effects of <italic>L-carnitine</italic> supplementation in water on selected blood plasma and hemogram parameters of broilers Table 4 Table 4. The effects of L-carnitine supplementation in water on selected blood plasma and hemogram parameters of broilers

Parameters Treatment groups

Control 100 mg/L L-carnitine 150 mg/L L-carnitine 200 mg/L L-carnitine 250 mg/L L-carnitine SEM p=

Blood plasma parameters

AST ( U/L) 292.68 238.90 275.28 290.03 249.06 12.788 0.456

ALT ( U/L) 7.10 4.14 5.68 5.30 5.88 0.392 0.091

ALP ( U/L) 2913.18 2875.25 3681.17 3012.12 2525.14 225.836 0.745

Total Protein(g/dl) 3.35 3.10 2.98 3.01 3.03 0.061 0.242

Cholesterol (mg/dl) 133.50 119.36 108.67 111.56 114.13 3.029 0.065

LDL(mg/dl) 14.49 10.40 9.60 12.31 10.80 1.187 0.696

HDL(mg/dl) 118.15^a 95.10^b 92.68^b 93.60^b 91.34^b 2.902 0.006

Triglyceride (mg/dl) 51.47a^b 37.14^b 41.00^b 34.33^b 60.38^a 2.616 0.012

Creatine Kinase (CK) (U/L) 15744.58^ab 9893.33^b 20395.20^ab 24622.83^a 8605.25^b 585.238 0.057

Glucose (mg/dl) 298.67^ab 283.57^b 286.50^b 285.44b 313.63^a 3.208 0.021

T3(pg/ml) 6.85 6.22 4.27 6.45 7.99 0.400 0.151

T4(ng/dl) 0.86^a 0.86^a 0.91^a 0.66^a 0.40^b 0.041 0.001

Hemogram parameters

RBC (1012/l) 2.98a 2.83ab 2.71b 2.89ab 2.71b 0.030 0.021

MCV (fl) 134.55 135.38 134.02 136.82 139.60 0.636 0.163

RDW ( %) 9.79 9.65 9.30 9.76 10.15 0.118 0.438

RDWa (fl) 77.55 77.39 74.22 79.16 82.65 1.041 0.339

Hematocrit (%) 40.19 38.34 36.30 39.64 37.78 0.475 0.083

Platelet (Thrombocyte) (109/l) 3.77 4.38 3.17 4.20 4.50 0.207 0.295

Hemoglobin (g/dl) 17.68 16.96 17.65 17.38 17.28 0.283 0.851

MCH (pg) 59.22b 59.89b 65.20a 60.02b 63.85ab 0.706 0.041

MCHC(g/dl) 43.97b 44.24b 48.70a 43.84b 45.68ab 0.496 0.025

*: Differences between group averages denoted by different letters in the same column are statistically significant (p<0.05). SEM: Standard error of difference between means.

Blood gas parameters. Blood gas, oximetry, electrolyte and metabolite were measured in the blood samples taken from 3 ascitic broilers and 3 healthy broilers from each subgroup. The effects of L-carnitine supplementation on blood gas paramaters of ascitic and healthy broilers are presented in table 5. L-carnitine supplementation in water did not have any significant effects on hematocrit, Sodium (Na), Potassium (K), Calcium (Ca), Plasma bicarbonate (HCO₃ p), Standart bicarbonate (HCO₃ pst), Base excess (C Base B) blood gas, electrolyte and metabolite values of ascitic and healthy broilers (p>0.05). On the other hand, Pouvoir hydrogen (pH), Partial pressure of carbon dioxide (pCO2), Partial pressure of oxygen (pO₂), Chlorine (Cl), Hemoglobin (Hb), Breathe carbon dioxide concentration (ctCO₂B), Partial pressure of carbon dioxide concentration (ctCO₂P), Anion K, Anion Gap, Oxygen saturation (SO₂) and Oxygen content (ctO₂) values were significantly affected by treatments (p<0.05). Blood pH value significantly decreased in ascitic broilers compared to healthy broilers.

Table 5. <bold>Table 5.</bold> The effects of <italic>L-carnitine </italic>supplementation in water on blood gas paramaters of ascitic and healthy broilers. Table 5. Table 5. The effects of L-carnitine supplementation in water on blood gas paramaters of ascitic and healthy broilers.

Blood gas parameters Treatment groups

Control 100 mg/l L-carnitine 150 mg/l L-carnitine 200 mg/l L-carnitine 250 mg/l L-carnitine SEM p=

pH Healthy 7.48^A 7.41 7.46^A 7.44^A 7.37^A 0.013 0.070

Ascitic 7.21^bB 7.42^a 7.32^abB 7.32^abB 7.29^bB 0.016 0.032

SEM 0.034 0.030 0.017 0.021 0.041

P 0.009 0.837 0.008 0.036 0.361

pCO₂ Healthy 37.00B 40.00 38.50B 40.00B 39.00B 0.880 0.904

Ascitic 66.00A 45.00 60.20A 61.86A 69.80A 2.472 0.122

SEM 4.195 2.915 3.425 3.431 6.088

P 0.014 0.349 0.019 0.019 0.042

pO₂ Healthy 38.50A 42.00 40.00 35.50^A 43.50^A 2.199 0.488

Ascitic 6.00^B 27.50 13.80 4.43^B 11.60^B 2.473 0.115

SEM 2.140 4.257 5.581 2.348 6.541

P 0.001 0.137 0.053 0.001 0.047

Hematokrit Healthy 31.00 31.00 40.00 31.50 29.00 2.604 0.406

Ascitic 41.67 34.00 45.80 43.57 39.00 3.215 0.946

SEM 2.273 12.083 1.706 3.130 8.804

P 0.102 0.651 0.128 0.111 0.570

Na Healthy 154.00 150.50 152.00 151.00 150.00 0.810 0.419

Ascitic 144.40 151.50 143.80 143.00 148.80 1.332 0.268

SEM 1.788 1.118 2.699 2.740 1.480

P 0.070 0.591 0.156 0.211 0.682

K Healthy 6.75 4.85 5.10 5.15 5.50 0.531 0.549

Ascitic 8.20 3.95 7.02 7.29 6.50 0.399 0.098

SEM 0.779 0.471 0.864 0.705 0.446

P 0.365 0.309 0.288 0.196 0.284

Ca Healthy 1.30 1.23 1.37 1.37 1.26 0.038 0.440

Ascitic 1.25 1.18 1.22 1.26 1.18 0.041 0.933

SEM 0.059 0.049 0.101 0.057 0.077

P 0.669 0.547 0.491 0.390 0.597

Cl Healthy 109.00^A 109.50^A 110.50 109.00 109.50 1.349 0.984

Ascitic 100.80^B 107.00^B 100.60 99.86 103.60 1.172 0.416

SEM 1.658 0.353 2.414 2.419 1.260

P 0.045 0.037 0.079 0.118 0.054

Hb Healthy 10.00 11.00 13.00 10.20 9.20^B 0.842 0.369

Ascitic 13.53 14.00 14.94 14.19 15.93^A 0.683 0.783

SEM 0.762 4.005 0.127 1.040 0.457

P 0.105 0.649 0.568 0.114 0.001

HCO3 p Healthy 27.10 24.45 27.00 26.75 23.35 1.316 0.633

Ascitic 25.52 28.40 30.12 31.10 31.88 0.811 0.073

SEM 1.532 1.645 1.085 1.451 1.774

P 0.605 0.231 0.185 0.200 0.050

HCO3 pst Healthy 24.20 24.20 27.05 26.50 23.00 0.756 0.199

Ascitic 21.43 26.55 24.88 25.36 26.20 0.728 0.260

SEM 2.184 1.151 0.768 1.161 1.579

P 0.519 0.285 0.191 0.656 0.307

C BaseB Healthy 0.10 0.50 3.50 2.90 -3.10 1.176 0.248

Ascitic -1.85 3.65 3.45 3.50 4.20 0.972 0.412

SEM 5.444 3.040 0.800 1.335 2.453

p 0.818 0.553 0.973 0.838 0.222

ctCO2B Healthy 21.50 22.55^B 23.95 24.75 22.00 0.863 0.483

Ascitic 24.63 25.10^A 27.48 28.70 29.60 0.795 0.231

SEM 2.017 0.145 1.037 1.156 2.014

P 0.442 0.006 0.128 0.151 0.094

ctCO2P Healthy 28.20 25.65 28.20 28.00 24.35^B 1.329 0.616

Ascitic 27.56 29.75 31.96 33.01 34.02^A 0.840 0.079

SEM 1.540 1.691 1.151 1.510 1.827

P 0.833 0.228 0.141 0.161 0.036

cCa Healthy 1.35 1.23 1.41 1.40 1.24 0.037 0.208

Ascitic 1.20 1.18 1.17 1.20 1.16 0.020 0.991

SEM 0.072 0.035 0.091 0.046 0.072

P 0.271 0.422 0.223 0.086 0.571

Anion K Healthy 22.80 21.40 19.60 20.40 22.90 0.961 0.533

Ascitic 26.28^a 20.05^b 20.10^b 19.33^b 19.82^b 0.689 0.007

SEM 2.137 0.506 0.698 0.988 1.463

P 0.498 0.200 0.717 0.625 0.311

Anion Gap Healthy 17.70 16.55 14.50 15.25 18.30 0.649 0.172

Ascitic 18.08^a 16.10^ab 13.08^ab 12.04^b 13.32^ab 0.755 0.050

SEM 1.403 0.617 1.314 1.366 1.340

P 0.907 0.657 0.588 0.305 0.103

SO2 Healthy 76.95^A 76.10 77.85^A 70.10^A 78.20^A 3.091 0.764

Ascitic 4.90^bB 52.00^a 21.10^bB 5.26^bB 18.98^bB 4.106 0.034

SEM 2.316 6.692 9.784 3.958 10.682

P <.001 0.125 0.026 0.001 0.031

ctO2 Healthy 10.80^A 11.50 14.20^A 10.05^A 10.35 0.779 0.225

Ascitic 1.47^B 10.40 4.14^B 0.84^B 5.28 1.003 0.070

SEM 0.889 3.080 1.888 0.598 2.736

P 0.023 0.824 0.035 0.000 0.344

*: Differences between group averages denoted by different small letters in the same row are statistically significant (p<0.05). **: Differences between group averages denoted by different capital letters in the same column are statistically significant (p<0.05). SEM: Standard error of difference between means.

<bold>DICUSSION</bold>

Similar to our live weight findings, 100 mg/kgL-carnitine supplementation to broiler rations with different energy levels (11); 900 mg/kg L-carnitine supplementation to 5% animal fat containing broiler rations (4); and 400, 600 and 800 mg/kg liquid and power L-carnitine supplementation to broiler rations (12) has been reported that L-carnitine additive has no significant effect on live weight gain at the end of the trial (p<0.05). Contrary to current research, there are studies reporting that L-carnitine contributes significantly to live weight gain. Parsaeimehr et al (13) reported that the addition of 300 mg/kg L-carnitine to rations containing different levels of animal fat significantly improved live weight gain. Jalali et al (14) reported significant increases in live weight at the end of the 35-day trial of L-carnitine addition (120 mg/kg) to rations containing soybean oil and sunflower oil. The differences observed among these research findings may be attributed to differences in rations, dose levels used, and combinations of other additives used along with L-carnitine supplementation. In summary, the fact that there is no statistical difference between the groups as revealed by the live weight data obtained at the end of the trial indicates that the doses of the L-carnitine supplementations used are not in the concentrations that will change the live weight value positively or negatively.

Murali et al (4) and Corduk et al (11) reported that L-carnitine supplementation in broiler rations had no significant effect on feed consumption. The results of these researchers are in line with our findings indicating that addition of different levels of L-carnitine in drinking water does not significantly affect feed consumption of broilers. On the other hand, there are also studies showing that L-carnitine supplement significantly affects feed consumption. Wang et al (15) reported that L-carnitine (100 mg/kg) supplement significantly reduced feed consumption in broilers raised at low ambient temperatures. Such differences between researches findings can be attributed to the dose levels of the L-carnitine supplement used, the ration energy levels and the animal species used. The fact that there is no statistical difference between the groups referred from the feed intake values obtained at the end of the study indicates that the L-carnitine dose levels used do not have a significant effect on appetite in broilers.

Murali et al (4); Taklimi et al (12) and Wang et al (15) reported that L-carnitine supplement had no significant effect on feed efficiency ratio in broilers. Likewise, Geng et al (16) conducted a study to determine the effects of L-carnitine and coenzyme Q10 additives on the immune system and growth performance of the broilers against ascites. L-carnitine was used at doses of 0, 75 and 100 mg/kg and coenzyme Q10 was used at doses of 0 and 40 mg/kg, respectively. As a result of the trial, the feed efficiency ratio in the group supplemented only with L-carnitine improved numerically. Michalczuk et al (17) reported that L-carnitine supplemented with drinking water (62.5 g/100 liters) improves the feed efficiency ratio numerically. The findings of these researchers are in agreement with the findings of this study. This consistency can be attributed to the fact that the levels of L-carnitine additives used do not affect feed consumption. Contrary to these findings, studies have shown that L-carnitine significantly contributes to the feed efficiency ratio. Sharifi et al (18) found that L-carnitine supplement (100 mg/kg) with reduced protein (3%) significantly improved feed efficiency. The differences observed between these research findings can be attributed to the differences in animal species and ration used.

Total water intake was numerically higher in the group supplemented with 100 mg/ L L-carnitine compared to the other groups by the end of the trial. This can be attributed to the fact that the group receiving 100 mg/l L-carnitine supplementation consumed higher amount of feed compared to the other groups. Although no statistically significant difference was found between the groups in terms of water consumption, it was noticed that water consumption decreased numerically with increasing levels of L-carnitine supplementation. This conclusion suggests that broilers will be of high importance in determining L-carnitine requirements.

In the current study, mortality rate in the group receiving 100 mg/l L-carnitine supplementation was found to be lower than that of the control group. The increase in ascites mortality rates in the 5th week towards the end of the trial can be attributed to the increased oxygen demand due to the increased live weights of the animals and the inability to meet them adequately, as well as the use of feed in pellet form. Zohair et al (19) reported that compared to powder feed, pellet feed triggers ascites in broilers raised at high altitudes. Ascites death rate in the current study is lower. This can be attributed to the fact that the animals were not subjected to cold stress, which triggers the ascites. In contrast to the present study, the rate of death due to ascites was identified as 3.75% for the group grown in normal temperature conditions; 12.5% for the cold stress group and 8.75% for the group exposed to cold stress and received L-carnitine (100 mg/kg) in the study conducted by Tan et al (20). These ascites death rates are lower than those obtained in the current trial.

Çördük et al (11) reported that L-carnitine supplementation in broiler rations did not significantly affect blood glucose, cholesterol and triglyceride levels. Likewise, total cholesterol, LDL and triglyceride levels (21); hemoglobin and MCV levels (22); serum cholesterol and LDL levels (23); blood glucose, LDL, cholesterol, triglyceride, and total protein levels (13) and serum hematocrit value (18) were not significantly affected by L-carnitine additive in broiler rations. These results are consistent with the findings of the present study.

Contrary to existing findings, Çördük et al (11) reported a significant increase in AST levels of broilers fed with high-energy rations. Şimşek et al (24) reported that WBC, RBC, hemoglobin and hematocrit values were higher in L-carnitine supplemented rats. Elgazzar et al (25) revealed that L-carnitine supplementation significantly reduced cholesterol, triglyceride, LDL, AST, ALT and ALP levels in New Zealand rabbits. Jali et al (14) found that L-carnitine supplement to rations containing soybean oil and sunflower oil significantly reduced triglyceride levels while significantly increasing blood total protein, cholesterol, HDL and LDL levels. The differences between these findings can be attributed to differences in the energy levels of the rations used, energy sources and animal material.

Geng et al (16) and Yousefi et al (26) reported that L-carnitine supplement significantly reduced the hematocrit value in broilers. In the current study, with L-carnitine supplement, the blood hematocrit value tended to decrease numerically though not statistically. The thyroid gland hormones (T3, T4) are directly related to the development of the animals as they increase the basal metabolism. When the thyroid gland is running poorly, there is a slow-down in the development of the animals due to the disorder that occurs in the basal metabolism (27). In the present study, plasma T4 levels were significantly reduced with high doses of L-carnitine supplement (250 mg/L). This may be related to the fact that the live weight gain is also found to be the lowest in this group.

While blood pH value was measured as 7.21 in ascitic broilers, it was measured as 7.48 in healthy broilers. Low dose of L-carnitine supplementation (200 mg/l) was observed to increase blood pH value in ascitic broilers (p<0.05). As expected, the pCO₂ value was found higher in ascitic animals compared to healthy animals, while the pO₂ value was found to be lower. However, these values were not resulted by statistically significant effects of L-carnitine supplementation. The lowest pCO₂ value for healthy animals was found to be 37.00 and the highest value for ascitic animals was 69.80. The highest pO₂ value for the healthy animals was 43.50 and the lowest value for the ascitic animals was 4.43. Van As et al (28) reported that while pCO₂ levels were significantly increased in ascites, pO₂ levels were significantly reduced. Hafshejani et al (29) reported a significant decrease in pH value in ascitic animals. The findings of these researchers are consistent with the findings of the present study. Although chlorine concentration value was not significant for all groups among all healthy and ascitic animals, it was statistically significant in control and the group receiving 100 mg/l L-carnitine supplementation. There was no statistical difference between the other treatment groups which can be attributed to the large intra-group variance. Concentrations of SO₂ and ctO₂ were higher in healthy animals, while ctCO₂P and hemoglobin concentrations were higher in ascitic animals (p<0.05). Blood hematocrit value was also increased numerically in ascitic animals. These results are in agreement with the findings of Tekeli (30). In broilers at high altitudes, SO₂ and FO₂Hb decrease oxygen saturation in blood and increase cTHb and Hctc (hematocrit) values, leading to ascites.

In conclusion, blood pH value significantly decreased in ascitic broilers compared to healthy broilers. L-carnitine supplementation was found to be beneficial in decreasing ascites (pulmonary hypertension) mortality rates. These positive effects can be achieved by using low doses of L-carnitine supplements. It is expected that L-carnitine supplementation in water of broilers which are fed on diets with lowered energy and protein contents can be more effective in reducing ascites mortality rates. More research is needed to confirm these benefits.

<bold>Conflict of interests</bold>

The authors reported no potential conflict of interest

Acknowledgements

The authors are grateful to Van Yuzuncu Yıl University (BAP Project No 2014 ZF-B179) for its financial and technical support

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Ingredients	Broiler starter diet (Days 1-10)	Broiler grower diet (Days 10-21)	Broiler finisher diet (Days 21-35)
Corn	411.07	450.70	460.74
Soybean meal (%46HP)	197.90	120.31	119.71
Full-fat soybean	140.00	160.00	160.00
Corn gluten flour (%60HP)	86.75	64.26	20.00
Rice (Broken)	40.00	40.00	40.00
Fish Flour (%53-60)	40.00	40.00	60.00
Sunflower meal (%36)	30.00	40.00	40.00
DCP (%18 P)	10.44	5.73	2.69
Chicken feather flour	10.00	10.00	10.00
Meat-bone flour (%35HP)	10.00	28.38	30.00
Corn extract (Full-fat)	-	20.00	20.00
Soybean oil	-	-	19.45
Marble powder	9.43	6.83	5.73
L-Lysine	4.12	4.20	2.99
Sodium bicarbonate	3.20	2.65	1.82
DL-methionine	2.21	2.09	2.01
Salt	1.40	1.21	1.60
Vitamin premixture1	1.00	1.00	1.00
Mineral premixture2	1.00	1.00	1.00
L-Threonine	0.88	1.04	0.66
Anticoccidial	0.60	0.60	0.60
Total	1000.00	1000.00	1000.00
Analysed nutrients (%)
Dry matter	89.44	89.19	89.26
Crude protein	25.70	23.74	20.95
Crude Fat	4.42	5.12	7.65
Crude cellulose	3.11	2.48	3.11
Crude cinder	5.81	5.45	5.07
Calculated nutrients (%)
ME (kcal/kg)	3020	3120	3220
Lysine	1.44	1.34	1.21
Methionine	0.68	0.64	0.57
Calcium	1.05	0.95	0.85
Phosphorus	0.81	0.74	0.70
Sodium	0.18	0.17	0.16
¹: Per 1 kg diet: 12.500.000 IU Vitamin A, 3.500.000 IU Vitamin D3, 100.000 mg Vitamin E, 4.000 mg Vitamin K3, 3.000 mg Vitamin B1, 8.000 mg Vitamin B2, 5.000 mg Vitamin B6, 20 mg Vitamin B12, 70.000 mg Niacin, 20.000 mg Pantothenic Acid, 2.000 mg Folic Acid, 250 mg Biotin, 100.000 mg Vitamin C, 125.000 mg Antioxidant. ²: Per 1 kg diet: 120.00 mg Manganese, 40.000 mg Iron, 110.00 mg Zinc, 16.00 mg Copper, 500 mg Cobalt, 1.250 mg Iodine, 300 mg Selenium.

Days	Treatment groups
Days	Control	100mg/L L-carnitine	150mg/L L- carnitine		200mg/L L-carnitine	250mg/L L-carnitine		SEM	p=
Live Weight, g
Day 0	46.61	46.53	46.34	46.63			46.59	0.235	0.995
Day 7	207.63^ab	210.84^a	209.93^a	200.51^b			213.95^a	1.396	0.005
Day 14	568.00^a	532.22^b	558.63^a	519.54^b			575.78^a	3.443	0.001
Day 21	1095.84	1088.81	1087.84	1065.59			1090.39	7.033	0.699
Day 28	1809.95^a	1808.51^a	1699.46^b	1737.04^ab			1715.75^ab	14.975	0.042
Day 35	2475.56	2484.30	2486.94	2456.42			2386.84	23.470	0.689
Feed consumption, g
Day 7	211.25	213.05	211.15		206.75	211.93		1.027	0.239
Day 14	458.82	510.28	478.78		465.85	497.79		9.417	0.256
Day 21	789.93	785.33	753.93		803.07	797.24		11.357	0.525
Day 28	1045.90	1050.59	968.00		999.40	961.50		16.481	0.179
Day 35	1181.19	1184.35	1151.04		1140.43	1240.48		36.835	0.847
Total	3687.08	3743.59	3562.95		3615.49	3708.93		44.302	0.541
Feed efficiency ratio, kg feed consumption/kg live weight gain
Day 7	1.31	1.31	1.29		1.35	1.27		0.019	0.577
Day 14	1.27	1.59	1.37		1.47	1.38		0.041	0.116
Day 21	1.51	1.41	1.41		1.46	1.54		0.031	0.392
Day 28	1.45	1.45	1.48		1.51	1.48		0.040	0.978
Day 35	1.60	1.67	1.49		1.38	1.58		0.068	0.525
Water consumption (ml)
Day 7	390.33	381.33	377.33		372.10	377.67		5.388	0.754
Day 14	1050.33	1074.67	1006.33		1018.33	1036.67		25.279	0.845
Day 21	1703.27	1847.93	1736.27		1715.47	1638.03		58.234	0.762
Day 28	2751.00	2915.00	2844.63		2601.70	2500.20		87.828	0.393
Day 35	3571.07	3940.40	3721.73		3248.40	3150.87		113.085	0.107
Total	9465.67	10159.33	9686.37		8956.03	8703.43		265.058	0.292
*: Differences between group averages denoted by different letters in the same row are statistically significant (p<0.05). SEM: Standard error of difference between means.

Treatment groups	Number of deaths from sscites	Mortality rate (%)
Control group	12	20.00
100 mg/l L-carnitine 150 mg/l L-carnitine	11 16	18.33 26.67
200 mg/l L-carnitine 250 mg/l L-carnitine	17 17	28.3328.33

Parameters	Treatment groups
Parameters	Control	100 mg/L L-carnitine	150 mg/L L-carnitine	200 mg/L L-carnitine	250 mg/L L-carnitine	SEM	p=
Blood plasma parameters
AST ( U/L)	292.68	238.90	275.28	290.03	249.06	12.788	0.456
ALT ( U/L)	7.10	4.14	5.68	5.30	5.88	0.392	0.091
ALP ( U/L)	2913.18	2875.25	3681.17	3012.12	2525.14	225.836	0.745
Total Protein(g/dl)	3.35	3.10	2.98	3.01	3.03	0.061	0.242
Cholesterol (mg/dl)	133.50	119.36	108.67	111.56	114.13	3.029	0.065
LDL(mg/dl)	14.49	10.40	9.60	12.31	10.80	1.187	0.696
HDL(mg/dl)	118.15^a	95.10^b	92.68^b	93.60^b	91.34^b	2.902	0.006
Triglyceride (mg/dl)	51.47a^b	37.14^b	41.00^b	34.33^b	60.38^a	2.616	0.012
Creatine Kinase (CK) (U/L)	15744.58^ab	9893.33^b	20395.20^ab	24622.83^a	8605.25^b	585.238	0.057
Glucose (mg/dl)	298.67^ab	283.57^b	286.50^b	285.44b	313.63^a	3.208	0.021
T3(pg/ml)	6.85	6.22	4.27	6.45	7.99	0.400	0.151
T4(ng/dl)	0.86^a	0.86^a	0.91^a	0.66^a	0.40^b	0.041	0.001
Hemogram parameters
RBC (1012/l)	2.98a	2.83ab	2.71b	2.89ab	2.71b	0.030	0.021
MCV (fl)	134.55	135.38	134.02	136.82	139.60	0.636	0.163
RDW ( %)	9.79	9.65	9.30	9.76	10.15	0.118	0.438
RDWa (fl)	77.55	77.39	74.22	79.16	82.65	1.041	0.339
Hematocrit (%)	40.19	38.34	36.30	39.64	37.78	0.475	0.083
Platelet (Thrombocyte) (109/l)	3.77	4.38	3.17	4.20	4.50	0.207	0.295
Hemoglobin (g/dl)	17.68	16.96	17.65	17.38	17.28	0.283	0.851
MCH (pg)	59.22b	59.89b	65.20a	60.02b	63.85ab	0.706	0.041
MCHC(g/dl)	43.97b	44.24b	48.70a	43.84b	45.68ab	0.496	0.025
*: Differences between group averages denoted by different letters in the same column are statistically significant (p<0.05). SEM: Standard error of difference between means.

Blood gas parameters		Treatment groups
Blood gas parameters		Control	100 mg/l L-carnitine	150 mg/l L-carnitine	200 mg/l L-carnitine	250 mg/l L-carnitine	SEM	p=
pH	Healthy	7.48^A	7.41	7.46^A	7.44^A	7.37^A	0.013	0.070
	Ascitic	7.21^bB	7.42^a	7.32^abB	7.32^abB	7.29^bB	0.016	0.032
	SEM	0.034	0.030	0.017	0.021	0.041
	P	0.009	0.837	0.008	0.036	0.361
pCO₂	Healthy	37.00B	40.00	38.50B	40.00B	39.00B	0.880	0.904
	Ascitic	66.00A	45.00	60.20A	61.86A	69.80A	2.472	0.122
	SEM	4.195	2.915	3.425	3.431	6.088
	P	0.014	0.349	0.019	0.019	0.042
pO₂	Healthy	38.50A	42.00	40.00	35.50^A	43.50^A	2.199	0.488
	Ascitic	6.00^B	27.50	13.80	4.43^B	11.60^B	2.473	0.115
	SEM	2.140	4.257	5.581	2.348	6.541
	P	0.001	0.137	0.053	0.001	0.047
Hematokrit	Healthy	31.00	31.00	40.00	31.50	29.00	2.604	0.406
	Ascitic	41.67	34.00	45.80	43.57	39.00	3.215	0.946
	SEM	2.273	12.083	1.706	3.130	8.804
	P	0.102	0.651	0.128	0.111	0.570
Na	Healthy	154.00	150.50	152.00	151.00	150.00	0.810	0.419
	Ascitic	144.40	151.50	143.80	143.00	148.80	1.332	0.268
	SEM	1.788	1.118	2.699	2.740	1.480
	P	0.070	0.591	0.156	0.211	0.682
K	Healthy	6.75	4.85	5.10	5.15	5.50	0.531	0.549
	Ascitic	8.20	3.95	7.02	7.29	6.50	0.399	0.098
	SEM	0.779	0.471	0.864	0.705	0.446
	P	0.365	0.309	0.288	0.196	0.284
Ca	Healthy	1.30	1.23	1.37	1.37	1.26	0.038	0.440
	Ascitic	1.25	1.18	1.22	1.26	1.18	0.041	0.933
	SEM	0.059	0.049	0.101	0.057	0.077
	P	0.669	0.547	0.491	0.390	0.597
Cl	Healthy	109.00^A	109.50^A	110.50	109.00	109.50	1.349	0.984
	Ascitic	100.80^B	107.00^B	100.60	99.86	103.60	1.172	0.416
	SEM	1.658	0.353	2.414	2.419	1.260
	P	0.045	0.037	0.079	0.118	0.054
Hb	Healthy	10.00	11.00	13.00	10.20	9.20^B	0.842	0.369
	Ascitic	13.53	14.00	14.94	14.19	15.93^A	0.683	0.783
	SEM	0.762	4.005	0.127	1.040	0.457
	P	0.105	0.649	0.568	0.114	0.001
HCO3 p	Healthy	27.10	24.45	27.00	26.75	23.35	1.316	0.633
	Ascitic	25.52	28.40	30.12	31.10	31.88	0.811	0.073
	SEM	1.532	1.645	1.085	1.451	1.774
	P	0.605	0.231	0.185	0.200	0.050
HCO3 pst	Healthy	24.20	24.20	27.05	26.50	23.00	0.756	0.199
	Ascitic	21.43	26.55	24.88	25.36	26.20	0.728	0.260
	SEM	2.184	1.151	0.768	1.161	1.579
	P	0.519	0.285	0.191	0.656	0.307
C BaseB	Healthy	0.10	0.50	3.50	2.90	-3.10	1.176	0.248
	Ascitic	-1.85	3.65	3.45	3.50	4.20	0.972	0.412
	SEM	5.444	3.040	0.800	1.335	2.453
	p	0.818	0.553	0.973	0.838	0.222
ctCO2B	Healthy	21.50	22.55^B	23.95	24.75	22.00	0.863	0.483
	Ascitic	24.63	25.10^A	27.48	28.70	29.60	0.795	0.231
	SEM	2.017	0.145	1.037	1.156	2.014
	P	0.442	0.006	0.128	0.151	0.094
ctCO2P	Healthy	28.20	25.65	28.20	28.00	24.35^B	1.329	0.616
	Ascitic	27.56	29.75	31.96	33.01	34.02^A	0.840	0.079
	SEM	1.540	1.691	1.151	1.510	1.827
	P	0.833	0.228	0.141	0.161	0.036
cCa	Healthy	1.35	1.23	1.41	1.40	1.24	0.037	0.208
	Ascitic	1.20	1.18	1.17	1.20	1.16	0.020	0.991
	SEM	0.072	0.035	0.091	0.046	0.072
	P	0.271	0.422	0.223	0.086	0.571
Anion K	Healthy	22.80	21.40	19.60	20.40	22.90	0.961	0.533
	Ascitic	26.28^a	20.05^b	20.10^b	19.33^b	19.82^b	0.689	0.007
	SEM	2.137	0.506	0.698	0.988	1.463
	P	0.498	0.200	0.717	0.625	0.311
Anion Gap	Healthy	17.70	16.55	14.50	15.25	18.30	0.649	0.172
	Ascitic	18.08^a	16.10^ab	13.08^ab	12.04^b	13.32^ab	0.755	0.050
	SEM	1.403	0.617	1.314	1.366	1.340
	P	0.907	0.657	0.588	0.305	0.103
SO2	Healthy	76.95^A	76.10	77.85^A	70.10^A	78.20^A	3.091	0.764
	Ascitic	4.90^bB	52.00^a	21.10^bB	5.26^bB	18.98^bB	4.106	0.034
	SEM	2.316	6.692	9.784	3.958	10.682
	P	<.001	0.125	0.026	0.001	0.031
ctO2	Healthy	10.80^A	11.50	14.20^A	10.05^A	10.35	0.779	0.225
	Ascitic	1.47^B	10.40	4.14^B	0.84^B	5.28	1.003	0.070
	SEM	0.889	3.080	1.888	0.598	2.736
	P	0.023	0.824	0.035	0.000	0.344
: Differences between group averages denoted by different small letters in the same row are statistically significant (p<0.05). *: Differences between group averages denoted by different capital letters in the same column are statistically significant (p<0.05). SEM: Standard error of difference between means.