The effects of omega-3 fatty acid used maternal rations during pregnancy on the fattening performances            of male kids

doi:10.21203/rs.3.rs-2227060/v1

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The effects of omega-3 fatty acid used maternal rations during pregnancy on the fattening performances of male kids

https://doi.org/10.21203/rs.3.rs-2227060/v1

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published 13 Jul, 2023

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In this study, fish oil was used as an omega-3 fatty acids source in pregnant goat’s rations in the different periods of pregnancy on mature male offsprings performance. Forty-seven male goat kids (84.6 ± 2.44 days or days old; 14.5 ± 3.09 kg body weight) were housed in individual pens and to evaluate live weight, feed consumption, serum biochemical parameters, carcass performance and meat quality characteristics for 56 days. Supplementation of fish oil to Anaç goats dam ration during the gestation periods decreased the fattening live weight and increased feed consumption (p=0.09), while body weight and feed conversion rates were not affected by experimental treatments (p=0.62, p=0.90). Fish oil increased serum AST, glucose, total protein, and globulin concentrations (p=0.02, p=0.01, p=0.03, p=0.02), while decreased heptadecanoic acid, oleic acid, linoleic acid, docosahexaenoic acid, and total mono- and polyunsaturated fatty acid concentrations in M. longissimus dorsi muscle (p=0.09, p=0.03, p=0.10, p=0.02, p=0.02, p=0.09). As a result, it has been thought that the use of liquid fish oil as an omega-3 source in goat’s ration during gestation may negatively affect the fetal development of male kids, but it has the ability to eliminate this negativity by improving post-weaning performance.

Maternal ration

fattening

fish oil

kid performance

The need for animal products has increased with the increasing human population. Breeding studies lasting many years in order to obtain and develop more productive breeds have an important place in providing meat and dairy products, which are the main products in animal production (Şengonca and Koşum, 2005). It has been suggested that maternal nutrition is one of the major determinants that contribute to the development of high productive breeds targeted in breeding studies. The methods applied in maternal nutrition can act in the same direction as the methods applied in breeding studies. Maternal nutrition applied during pregnancy has an important role, particularly, in providing placental - fetal development, and also it affects the offspring’s lifespan and postnatal productivity (Belkacemi et al, 2010). Since, maternal feeding management during pregnancy has a potential lifelong impact on the health of animals and is a viable method for increasing the production of offspring, proper maternal nutrition is important for food animals breeding (Garcia et al. 2014; Batistel et al. 2019).

The lipids in the nutrition of farm animals has been studied under many titles such as postnatal growth performance (Sampelayo et al, 2006), influencing the metabolism by regulating gene expressions (Jump, 2004), meat quality and meat production (Wood et al, 2003). It is thought that maternal fatty acids may cause epigenetic modifications (Heerwagen et al., 2010) by acting like metabolic sensors in the regulation of genes involved in energy oxidation and storage (İnnis, 2011). It has been reported that the presentation of nutrients that activate various signaling pathways and receptors that govern the myogenesis and adipogenesis processes in the fetal period to the mother at appropriate rates and amounts can activate muscle tissue and adipose tissue formation, respectively, in the fetus. It is known that the lipid taken with the diet in the early period of pregnancy regulates the lipid metabolism of the fetus (Fernandes et al., 2012).

In normal fetal development, long-chain polyunsaturated fatty acids, especially arachidonic acid (AA), eicosapentanoeic acid (EPA) and DHA, are important in terms of physiological roles (metabolic, energetic and structural), and play an important role during developmental periods (Mennitti et al., 2015; Cetin et al., 2009).There are the evidences indicating the use of Omega 3 PUFA in the maternal diet can regulate the immune responses of the offspring and stimulate energy metabolism markers and epigenetic changes that influence the growth and development of the offspring in the postnatal period (Coleman et al. 2018; Nickles et al. 2019). Eicosapentaenoic acid (EPA) and Docosahexaenoic acid (DHA) found in fish oil, which is used as a source of omega-3 (n-3) fatty acids, have bioactive properties (Pickard et al. 2005; Capper et al. 2006). Based on these points, in the current thisstudy, it washypothesized that the use of fish oil, which is an important omega-3 source, in the maternal ration during pregnancy in goats may have an effect on the growth performance and yields of the offspring and their further generations.In this study, the effect of using fish oil in the maternal ration at different stages of pregnancy on the fattening performance of male kids after weaning was investigated.In the literature, the effects of using omega-3 fatty acids in the diet in dams and offspring are mostly observed in short-term (in the prepartum and postpartum periods, performance of the offspring until weaning) studies. The present study is unique as it investigated the effect of omega-3 fatty acids on the adulthood performance of offspring.

Animals and Study Design

Crossbreed Colorful German Noble Goat x Hair Goat (75%Colorful German Noble Goat and 25% Hair Goat), which were included in the synchronization and mating program, received fish oil as an omega-3 fatty acids source (Table 1) in their rations at different periods of pregnancy from mating to birth (Includes two periods containing: first half of pregnancy: period between mating and 75^th day of pregnancy, second half of pregnancy: 76^th day of pregnancy and between kidding). Achieved newborn male kids were distributed into four groups as the groupwhich received protected fat (PF) throughout gestation (PF - PF), the group that receivedprotected fat in the first half of the gestation - fish oil (FO) in the second half of the gestation (PF - FO), the group that received fish oilthroughout gestation (FO – FO) and the group that received fish oil in the first half of gestation – protected fat in the second half of the gestation (FO – PF).

The animal material consisted of 47 male kids aged 84.6 ± 2.44 days (mean ± standard deviation) having 14.5 ± 3.09 kg body weight.From 57 goats with an average body weight of 50.8 kg, male kids were obtained.This study, which investigated the effects of feeding the dams with diet containing omega-3 fatty acid at different periods of gestation, on the fattening performance, serum biochemical parameters and carcass characteristics of male kids, lasted for 56 days.

Forty-seven male goat kids (84.6 ± 2.44 days or bearth; 14.5 ± 3.09 kg body weight) were placed in pens (6 m x 12 m; width x length) according to the groups formed by maternal nutrition (PF – PF, PF – FO, FO – FO and FO – PF). Within these pens, 3 subgroups consisting of 3-5 kids in each were formed.TMRs (Total Mixed Ration) consisting of concentrate feed and dried alfalfa hay were used in the fattening of male kids.In the total mixed ration, the ratio of concentrate feed: roughage was arranged as 85: 15. The ingredients and nutrient composition of the concentrate feed and TMR used in the experiment are given in Tables 2 and 3, respectively.The water requirement of the kids was met ad libitum with the help of plastic buckets fixed to the compartments.

Determination of Live Weight and Live Weight Changes

Fattening male kids were individually weighed weekly before morning feeding. Live weight gain of animals were calculated by subtracting the previous weight from the last weighing and dividing the obtained value by the number of the elapsed days.

Determination of Feed Consumption and Feed Conversion Efficiency

In the study, TMR consisting of concentrate feed and dried alfalfa hay was filled in 45 kg feed bags.Kids were fed twice a day, at 08:00 and 17:00, and care was taken to ensure that at least 5% of unconsumed feed was left in the feeders on a daily basis.On the day when the feed consumption was determined, the remaining feed in the feeders, the feed spilled around the feeder and the amount of feed remaining in the bag were collected and subtracted from the initial weight of 45 kg. Feed conversion efficiency was determined by dividing feed consumption by live weight gain.

Determination of Biochemical Parameters

Individual blood samples were taken from the vena jugularis with serum tubes containing gel (9 ml, Ayset, Turkey) before morning feeding at the beginning (day 1), middle (day 28) and end (day 56) of the fattening period.The collected blood samples were transported to the Department of Feeds and Animal Nutrition Laboratory rapidity, where they were centrifuged at 4°C and 4000 rpm for 15 minutes (Universal 320R, Hettich, Germany), and the obtained sera were transferred into 1.5 ml Eppendorf tubes with the protocol number, and they were stored at -20°C until analyses. Aspartate aminotransferase (AST), alanine aminotransferase (ALT), gamma-glutamyl transferase (GGT) and alkaline phosphatase (ALP) activities, albumin, total protein, total cholesterol, glucose, triglycerides, magnesium, calcium concentrations in sera were detected on a biochemistry analyzer (BS-120 Vet, Mindray, China) with the commercially available kits provided by the manufacturer of the analyzer.Globulin level was calculated by subtracting albumin value from total protein value.

Collection of Data Related to Carcass and Meat Quality

At the end of the fattening period, 5 kids from each treatment group having live weight close to mean live weight were slaughtered in a private slaughterhouse.After slaughter, slaughter weight, skin, heart + lung (set), liver and hot carcass weights were recorded. The carcasses were stored at +4°C for 24 hours in a cold storage room. At the end of this period, cold carcass, fat around kidneys, cervical (neck), thigh, shoulder head, arm, lumbar (waist) and flank weights were determined (Darcan et al, 2006; Atay et al, 2007).

Color, pH, texture and fatty acid analyses were performed on 15 gr muscle samples taken from the Longissimus dorsi muscle at 1 hour after slaughter. In color analysis, L*, a*, b* values were determined by using Konika Minolta CM-5 instrument according to the method indicated by Calder (2003).

Texture analysis in the meat ofkid was performed using the TA-XT2 plus model (Stable Micro Systems, Godalming, UK) texture analyzer according to the method of Bourne (1978).Warner-Bratzler probe was used for shear force, hardness and adhesivenessparameters were determined using P/50 cylindricalprobe using 50kg load cell. Measurements were made using an immersion depth of 60% of the original height at a speed of 20 cm/min and an initial sensing force of 10 g.The samples used in the analysis were taken using a sampling apparatus with a certain diameter, and 6 replications were applied. At the end of testing, the values of hardness and external adhesiveness of tissue were determined.

Analysis of Fatty Acid Profile in Meats

Crude fat content and fatty acid profile were determined in meat samples taken from M. Longissimus dorsi of kids slaughtered at the end of the fattening period.Fat analysis in the samples was carried out according to the method applied by Bligh and Dyer (1959). The fatratio was calculated with the following formula:

Amount of fat (%)= {[final weighing (g) - first weighing (g)] x 100}: Amount of sample (g)

Fatty acid methyl esters (FAME) from extracted fatweredetermined according to the method indicated by Ichihara et al. (1996).

Fatty acid analysis was performed on GC Clarous 500 instrument (Perkin–Elmer, USA) using a flame ionization detector and an acid silicide salt tube SGE (30 m x 0.32 mm ID x 0.25 lm BP20 0.25 UM, USA).

Nutrient Analysis of the Feeds Used in the Experiment

Samples were taken from the roughage and mixed feed used in the trials, and dry matter, crude protein, crude oil and crude ash analyses were performed according to AOAC (1998). Neutral detergent fiber (NDF) and acid detergent fiber (ADF) analyses were carried out with filter bag technique on fiber analyzer (Ankom200 Fiber Analyzer, ANKOM Technology Corp., NY) using temperature resistant α-amylase and sodium sulfite as indicated by Vansoest et al. (1991).

Statistical Analysis

The SAS package program (SAS Institute Inc. 2014) was used in the statistical analysis of the collected data.The normal distribution tests for the data were performed with the Shapiro-Wilk test using the UNIVARIATE procedure, and the GLIMMIX (Stroup et al. 2018) procedure was used in the analysis. Statistical analyses were based on repeated measurement data analysis, and Combined Symmetry (CS), Heterogeneous Combined Symmetry (CSH), First Order Autoregressive (AR(1)), First Order Autoregressive with Heterogeneous Variance Structures [ARH(1)], Unstructured, First Order Ante dependence[ANTE(1)], Distance Exponent [SP(POW)] and Moving Average First Order Autoregressive [ARMA (1, 1)] were used as covariance structure (Çetin, 2009; Çetin and Bek, 2019).The smallest Akaike information criterion (AIC) was used to select the most appropriate covariance structure for the data.In the selection of this criterion, it was aimed to have the lowest Type 1 error.

In the statistical models, the maternal nutrition (rations provided to the goats during pregnancy: PF - PF, PF - FO, FO - FO and FO - PF), time (day, week or month) and maternal nutrition x time interaction were found to be fixed effects.In examination of fattening performance of male kids, initial live weight was assigned to the statistical model in the analysis of performance data, and slaughter weight was assigned to the statistical model in the analysis of carcass and fatty acid profile.

In all statistical analyzes, it was accepted as significant if the p value was less than ≤0.05, and as an increasing or decreasing trend if the p value was 0.05 < P ≤ 0.10. The least squares mean and the pooled standard errors calculated for these means are used in the tables.Pooled standard errors were calculated by multiplying the n of each group with the standard error of that group, then finding the grand total and then dividing this value by the total number of n.Tukey's multiple comparison test was used to compare the means in cases where the p value was ≤0.05.

Fattening Performance of Male Kids

The effect of the feeding system applied to the dams during pregnancy on the live weights of the fattening male kids was not statistically significant (p>0.05, Table 4). The common effect of week and maternal nutrition (MN) x week on body weights was found to be statistically significant (p<0.01, Figure 1a).At the end of the fattening period (5^6th day), the highest body weight (25.2 kg) was reached by male kids born todams fed with ration containing protected fat throughout gestation (PF– PF). The lowest live weight (24.3 kg) was determined in kids born to dams fed with diet containing fish oil (FO – FO) throughout gestation. It was observed that the maternal nutrition affected the live weight gain of the fattened male kids (p= 0.050). It was determined that there was a 13% difference between the groups with the highest and lowest body weight gain (PF – PF treatment group vs. FO – FO treatment group). The common effects of Week and MN x Week on the body weight gains of the groups were found to be statistically significant (p<0.01, Figure 1b).The feed consumption of the groups tended to be statistically different (p= 0.090). During the fattening, the highest daily feed consumption was found in male kids whose maternal nutrition was PF - PF (865.7 g / day), and the lowest feed consumption was found in kids whose maternal nutrition was FO - PF (794.6 g / day).Feed consumption was significantly affected (p< 0.01, Figure 1c for both) by the common effects of Week and MN x Week.

The maternal nutrition did not affect the feed conversion rate of the male kids (p>0.05) and the feed utilization during the fattening period was approximately 4.57 kg feed intake per 1 kg live weight gain in all groups. On the other hand, feed conversion ratio was affected significantly (p<0.01 and P <0.05, respectively, Figure 1d) from the common effects of Week and MN x Week.

The use of omega-3 fatty acid source in the rations of dams during pregnancy did not affect serum liver enzymes, ALT and GGT, as well as ALP activities of male kids (p>0.05, Table 5). It was determined that maternal nutrition had a statistically significant (p< 0.05) effect on serum AST activity in male kids.The serum AST activity is the highest (119.3 IU/dl) in kids born to dams fed omega-3 fatty acids rich diet i.e. supplemented with fish oil (FO – FO) throughout gestation, and the lowest (94.0 IU/dl) in male kids born to damson PF – FO feeding system. It was observed that the combined effect of MN x Week on serum AST activity was also statistically significant (p<0.05, Figure 2).The serum glucose concentrations of male kids (Table 5) were affected by the feeding system applied during the gestational period (P <0.01) and the highest level (62.3 g/dl) was found in the kids born to dams on the FO – PF feeding system.In terms of this variable, the lowest level (45.5 g/dl) was observed in male kids born to dams receiving FO – FO ration throughout gestation.Feeding during pregnancy did not affect serum total cholesterol and triglycerides levels (p>0.05).

Feeding with a diet containing fish oil throughout gestation affected the serum total protein concentration of kids (p<0.05).The highest value (5.89 g/dl) was observed in kids born to dams who received fish oil throughout gestation (FO – FO), whereas the lowest value (5.39 g/dl) was found in the group receiving protected fat in the first half of the gestation and fish oil in the second half of the gestation (PF – FO).A similar effect (p< 0.05) valid for the globulin concentration found by calculation (globulin = total protein – albumin). Maternal nutrition had no effect on serum Ca and Mg concentrations (p >0.05). It was determined that the mean values for these minerals were 10.5 mg/dl and 6.98 mg/dl, respectively.

The feeding system applied to dams during pregnancy tended to affect the hot and cold carcass weights of male kids statistically (P= 0.078 and P= 0.084, respectively, Table 6). The hot carcass weights of male kids born to dams fed with diets containing fish oil throughout gestation was the highest (11 kg). However, the male kids born to dams that received fish oil in the first half of gestation and protected fat in the second half of the gestation had the lowest hot carcass weights (9.86 kg).

Other examined variables (skin, set, heart, neck, flank, shoulder head, thigh, arm, waist, kidney weights) were not affected by the maternal nutrition (p>0.05).In addition, gestational feeding did not affect the shear force, tenderness, juiciness and pH values of the meat quality characteristics of kids (p>0.05 for all variables).

In the present study, it was determined that the maternal nutrition was not statistically effective (P >0.05) on the meat quality characteristics of male kids. The effect of gestational feeding on M. longissimus dorsi fatty acid profile is given in Table 7. It was determined that the use of fish oil in the diet during pregnancy tended to affect heptadecanoic acid concentrations (C17:0 and cis-10, C17:1) (p= 0.089 and p= 0.097, respectively).

In addition, the erucic acid concentration tended to be affected by the gestational feeding system (p= 0.072). The highest concentration (1.38 g/100 g fat) was observed in kids born to goats who received protected fat throughout gestation, whereas the lowest concentration (0.68 g/100 g fat) was determined in the kids born to goats, who received fish oil in the first half and protected fat in the second half of gestation.The lowest oleic acid concentration was determinedinkids born from to dams on diets either containing preserved oil (32.9 g/100 g oil) or fish oil (32.4 g/100 g oil) (p< 0.05) throughout gestation.

It was determined that the linoleic acid concentrations of the kids tended to differ slightly (p = 0.100).The highest (6.18 g/100 g fat) and the lowest (4.76 g/100 g fat) concentrations of linoleic acid were found in kids born to dams on the diet containing protected fat throughout gestation and in kids born todams consuming rations containing protected fat in the first half and fish oil in the second half of gestation, respectively.The docosahexaenoic acid concentration was also found to be high in kids of goats fed diet containing protected fat throughout the gestation period (p<0.05).Approximately 44% lower values in this fatty acid concentration were determined in other groups.

There was no statistically significant difference between the groups in terms of total saturated fatty acid (p>0.05).There was a difference between the groups concerning monounsaturated fatty acids (p<0.05), and the highest monounsaturated fatty acid concentration (40.4 g/100 g oil) was observed in the group that received protected fat in the first half and fish oil in the second half of gestation. The total polyunsaturated fatty acid concentration was the highest in the PF – PF group (6.37 g/100 g fat) and there was a tendency level statistical difference (P=0.090) between the groups in terms of this variable.

In the fattening study conducted by Darcan and Cankaya (2008) in male kids for 2 months, the reported daily live weight gain was lower than the present study (132.5 g/day vs. 202.4 g/day).Kaliber (2012) also reported the daily live weight gain of 90 g/day for doeling.Manso et al. (2011) reported that there was no statistical difference in the birth weight of lambs born to ewes fed with different fat sources (palm oil, olive oil, soy or flaxseed oil). Valezquez et al. (2022) determined that the birth weight and 30-day-old live weights of the offspring of ewes fed with the addition of calcium salts-processed EPA and DHA and protected methionine to their rations during late pregnancy were similar. However, there are studies reporting that the use of fat in the diet during pregnancy has a positive effect on the offspring.Gomez-Cortes et al. (2014), in their study, found no difference in birth weight of lambs born to ewes whose diets were supplemented with 70 g of palm oil (protected oil) treated with calcium salts daily or 128 g of flaxseed daily (a source of omega-3 fatty acids rich in α-linolenic acid). and they reported that lambs of ewes in the flaxseed treatment group were heavier than the lambs of ewes on the diet with protected fat (4.54 kg vs. 3.94 kg). Alshdaifat (2017) determined a higher birth weight of lambs born from Awassi sheep fed with fish oil in the ration during gestation than the other treatment groups (5.0 kg versus 4.3 kg).Mahboub et al. (2013) also claimed that the use of ration containing fish oil in the late stages of pregnancy in sheep may increase the birth weight of lambs. High birth weight can positively affect weaning body weight and fattening performance in the future.Valezquez et al. (2022) reported no difference between the treatment groups in terms of birth weights of lambs born from sheep receiving the diet supplemented with EPA and DHA processed with calcium salts and protected methionine in the late stage of gestation. However,these authors determined that weaning weight of the offspring in Methionine-Fish oil (M-FO) treatment group at 60 days of age was lower than the live weight of the lambsin the methionine (M)and fish oil (FO)group.In the present study, when the initial live weight of kids considered, it was seen that the male kids born tothe goats in the FO – FO and FO – PF groups were lower than the male kids born to the goats in the PF – PF and PF – FO groups.This indicates that the use of fish oil as a source of omega-3 throughout gestation or the use of fish oil in the first half of gestation may adversely affect fetal development.As it is known, in ruminants, active lipid sources (such as fish oil which was used in the present study) can reduce the digestibility of the feed by having a negative effect on the rumen microbial population and ruminal fermentation.On the other hand, the development of muscle fibers in ruminants takes place in the first half of pregnancy (Wilson et al., 1992).In this case, it was evaluated that the negativities experienced in fetal development during the pregnancy period led to the problems seen in the fattening period. At this point, it should be emphasized that although protected oil has a more positive effect on the live weight gain and feed consumption of the groups compared to fish oil, there is no difference between the live weight and feed conversion ratio.It has been evaluated that this situation is due to the numerically better feed efficiency rates of male kids born from goats fed with rations containing fish oil because of consuming less feed for kg live weight gain (approximately 3%). It was reported that maternal PUFA supplements regulate the glucose metabolism of the offspring, and changes in the live weights of the offspring may be due to the unpaired glucose-insulin system (Nickles et al.2019). On the other hand, Annett et al. (2009) reported that the addition of fish oil to the ration in the late pregnancy period in 55 primiparous and multiparous ewes of Texel×Greyface crossbred did not affect the live weight gain of the lambs. Similarly, Valezquez et al. (2022), in their study on sheep, reported no difference in feed intake, daily live weight gains and feed conversion rate of the lambs born toewes fed with the addition of protected methionine and EPA and DHA treated with calcium salts to their rations during the late pregnancy period. Consistent with the present study, it was reported that the use of flaxseed oil or fish oil in the diet during the prepartum period did not affect the blood serum GGT and total cholesterol concentrations of calves (Ataözü, 2019).In the present study, although the effect of maternal nutritionon serum AST activities of male kids were statistically significant, it was reported that AST activity values were within normal reference limits(Jackson and Cockcroft, 2002). In this study, the lowest serum glucose levels were detected in offspringofgoats who received fish oil throughout gestation. In contrast, Rosa-Velazquez et al. (2021) reported the highest glucose level in the weaned offspring of the treatment group receiving the diet supplemented with EPA and DHA containing Ca salts in their last stage of pregnancy. It was reported that there was no difference in glucose levels in offspring of the treatment group fed with PUFA supplements compared to the treatment group that received saturated fat during gestation (Carranza-Martin et al. 2018). Similarly, it has been reported that there is no difference in glucose concentrations at 2 months of age in lambs of ewes fed with monounsaturated fatty acids (Oleic acid) or polyunsaturated fatty acids (EPA and DHA) enriched with Ca salts in the last 50 days of gestation (Coleman et al, 2018). Consistently, Valezquez et al. (2022), in their study performed on sheep, reported that the addition of omega-3 fatty acids and methionine to the maternal ration had no effect on the plasma glucose concentrations of the fattening calves. In the present study, although there was no statistically significant difference in the group fed diets containing fish oil (FO– FO) throughout gestation, compare to other treatment groups, presence of higher triglycerides levels (48.4 g/dl) may be related to globulin levels. It was reported that α and β globulins among serum proteins in goats carry fats and γ globulins carries antibodies (Nagy et al, 2015). However, Valezquez et al. (2022), in their study designed by adding omega-3 fatty acids and methionine to maternal rations in sheep, determined no difference between the treatment groups in terms of plasma NEFA concentrations during the fattening period of the offspring.

In this study, although male kids born to dams receiving diet containing fish oil throughout the gestation had the lowest body weight (24.3 kg), hot carcass weight tended to be higher (11.0) than the other treatment groups at the end of the fattening period. One of the reasons for this may be the increased DNA methylation in the small intestines, an increase in mRNA, and protein expression of amino acid transporters in the small intestines in male kids born to damsreceiving fish oil during pregnancy (Rosa-Velazquez et al. 2020).The heavier hot carcass in this group may be related to the increase in content of skeletal muscle phospholipids that is followed by an increase in the membrane insulin number and insulin binding capacity, thus leading to higher food intake and skeletal muscle growth due to omega-3 fatty acids in the diet as suggested by Liu et al. (1994) in their rat study. Such mechanisms may positively affect the hot carcass weight due to the increase in nutrient absorption. In consistent with the present study, Valezquez et al. (2021) reported that hot carcass weight of male lambs born to mothers fed the diet supplemented with EPA and DHA source in the last period of pregnancy tended to be higher. It has also been reported that the hot carcass weight of the kids born to the goat in the PUFA treatment group receiving EPA and DHA was higher than the kids born to goat in the treatment group receiving saturated and monounsaturated fatty acids enriched with Ca salts (Carranza-Martin et al. 2018).Higher hot carcass weight in male calves of cows fed diet supplemented with PUFA during pregnancy was also reported by Marques et al. (2017). On the other hand, it was reported that the addition of flaxseed to the rations of lactating sheep or the addition of flaxseed to the concentrated feed of lambs had no effect on hot and cold carcass weights (Berthelot et al, 2012). However, Nudda et al. (2014) showed that cold carcass weight of lambs of ewes in the flax/control treatment group tended to be lower than the lambs born to ewes in the flax/flax and control/control treatment groups when flaxseed was used in the ration in the last period of pregnancy and early lactation.

Manso et al. (2011) reported that the addition of 3% vegetable oil (palm oil, olive oil, soy or flaxseed) into the rations of lactating sheep did not affect the intramuscular fatty acid composition, carcass components and non-carcass components of suckling lambs.. Related to this issue, Berthelot et al. (2012) determined that the addition of flaxseed to the rations of lactating sheep or the addition of flaxseed to the concentrated feed of lambs did not cause any difference in terms of meat color characteristics.In addition, the use of extruded flaxseed in the diet during the last period of pregnancy and lactation did not change the meat color and tenderness characteristics of lambs.

No difference was found in terms of intramuscular saturated fatty acids in lambs sucking the milk of sheep fed with different fat sources during the lactation period (Gallardo et al, 2014). On the other hand, the lowest level of stearic acid (C18:0) concentration in subcutaneous fat and muscle was found in lambs receiving the milk of ewes that consume the rations containing palm oil, which is saturated, compared to olive, soy or flaxseed oils (Manso et al, 2011). Similarly, when compared to diets containing α-linolenic acid rich sources such as flaxseed, it has been observed that the palmitic acid (C16:0) concentration is high in lambs sucking the milk of mothers consuming rations that do not contain oilseeds (Berthelot et al. 2012). Since the studies in the literature reported here were predominantly conducted before weaning, insufficient or absent rumen biohydrogenation should be taken into account. In the present study, because male kids are fattened after weaning, it was also evaluated that rumen biohydrogenation may have a different course.In addition, it was thought that the higher feed consumption of kids born to dams, especially, in the PF – PF and PF – FO group than that of the kids born to dams in the FO – FO and FO – PF group caused the differences in the fatty acid profile.

Consumption of fish oil-containing rations during pregnancy increased the hot and cold carcass weights of male kids. However, heptadecanoic acid (C17:0 and cis-10, C17:1), oleic acid, linoleic acid, docosahexaenoic acid, total mono and polyunsaturated fatty acid concentrations in M. longissimus dorsi were higher in the male kids born to dams who fed protected fat supplemented diets during gestation.

As a result of the present study, it can be suggested that the use of liquid fish oil as an omega-3 source in the feeding of dams at different stages of pregnancy may negatively affect the fetal development of male kids, but it has the ability to eliminate negativity by improving post-weaning performance.

Acknowledgements

The article was extracted from the Ph.D. thesis prepared by İbrahim EREZ, under supervision of Prof. Dr. Uğur SERBESTER.

Authors’ contributions Conceptualization: İbrahim Erez, Uğur Serbester; Data Curation: İbrahim Erez, Formal analysis and investigation: İbrahim Erez; Methodology: İbrahim Erez; Project administration: İbrahim Erez, Resources: İbrahim Erez ; Software: Uğur Serbester; Validation: Uğur Serbester; Supervision:Uğur Serbester; Writing - original draft preparation: İbrahim Erez; Writing - review and editing: İbrahim Erez, Uğur Serbester.

Funding The authors did not receive support from any organization for the submitted work.

Data availability Data are available from the corresponding author on request.

Ethics approval Protocol (2-4, 2015) was approved by the experimental animal ethics committee of Çukurova University. The study was carried out in the research and application farm livestock department, agricultural faculty, Çukurova University, Turkey

Conflict of interest There is no conflict of interest between the authors.

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Table 1. Composition of maternally used protected fat or fish oil as the main source of fatty acids (g/100 g oil)

Fatty acids (%)	Protected fat²	Fish oil¹
DHA	-	26.7
EPA	-	9.75
Linoleik asit	-	1.81
Miristik asit	1.18	5.02
Oleik asit	6.90	17.49
Palmitik asit	62.11	19.85
Palmitoleik asit	-	5.73
Stearik asit	29.83	4.57
Arasidonik Asit	-	0.08
Linolenik asit	-	0.88

¹Liquid fish oil produced from salmon,²: Fractionated triglyceride structure of palm oil

Table 2. Ingredients and nutrient composition of concentrate used in the fattening of male kids (dry in air)

Ingredients of feed	%
Corn	41.4
Barley	11.3
Vibrotal	3.0
Soy bean meal (with 48% crude protein)	17.4
Wheat bran	7.5
Corn distillers dried grains with soluble (DDGS)	15.1
Fractionated oil	1.5
Salt	0.8
Vitamin-mineral mixture¹	0.1
Sodium bicarbonate	0.8
Lime	1.1
Nutrient composition	%
Dry matter	89.53
Crude protein	18.30
Acid Detergent Fiber	6.64
Neutral Detergent Fiber	20.01
Crude fat	3.83
Crude ash	6.90

¹ Provided per kilogram of vitamin-mineral mixture: 15.000.000 IU vitamin A, 3.000.000 IU vitamin D3, 30.000 mg Vitamin E, 150.000 mg Niacin, 10.000 mg Cu, 800 mg I, 150 mg Co, 150 mg Se, 50.000 mg Mn, 50.000 mg Fe, 50.000 mg Zn, 6.800 mg organic Mn, 1.400 mg organic Cu, 6.800 mg organic Zn, 6.800 mg organic Fe, 50 mg organic Se.

Table 3. Ingredients and nutrient composition of Total Mixed ration in the fattening of male kids (dry in air)

Ingredients of feed	%
Corn	35.2
Barley	9.6
Vibrotal	2.6
Soy bean meal (with 48% crude protein)	14.8
Wheat bran	6.4
Corn distillers dried grains with soluble (DDGS)	12.8
Fractionated oil	1.3
Salt	0.7
Vitamin-Mineral mixture¹	0.09
Sodium bicarbonate	0.7
Lime	0.9
Alfalfa hay	15.0
Nutrient composition	%
Dry matter	89.48
Crude protein	17.67
Acid Detergent Fiber (ADF)	10.72
Neutral Detergent Fiber (NDF)	23.17
Crude fat	3.51
Crude ash	7.25

¹ Provided per kilogram of vitamin-mineral mixture:: 15.000.000 IU vitamin A, 3.000.000 IU vitamin D3, 30.000 mg Vitamin E, 150.000 mg Niacin, 10.000 mg Cu, 800 mg I, 150 mg Co, 150 mg Se, 50.000 mg Mn, 50.000 mg Fe, 50.000 mg Zn, 6.800 mg organic Mn, 1.400 mg organic Cu, 6.800 mg organic Zn, 6.800 mg organic Fe, 50 mg organic Se.

Table 4. The fattening performances of male kids born to dams receiving omega-3 fatty acids in their rations at different stages of gestation

	Maternal Nutrition (MN)¹				SEM²	P³
	PF – PF	PF – FO	PF – FO	FO – PF	SEM²	MN	Week	MN x Week
n	11	12	13	11
Initial live weight (kg)	15.4	15.1	13.5	14.0	0.79	0.329	-	-
Live weight (kg)	20.6	20.6	20.3	20.0	0.36	0.623	<0.01	<0.01
2. week	17.6	17.8	17.4	16.7	0.29
4. week	20.1	20.1	20.0	19.4	0.39
6. week	22.7	21.7	21.7	21.9	0.51
8. week	25.2	24.9	24.3	24.8	0.58
Live weight gain(g/day)	214.4	213.9	189.9	191.3	8.00	0.050	<0.01	<0.01
2. week	293.8	311.4	257.6	171.8	24.39
4. week	180.4	146.0	187.0	198.7	21.88
6. week	242.4	113.1	104.7	213.8	29.85
8. week	217.6	162.7	125.1	230.5	30.00
Total live weight gain (kg)	10.8	10.4	9.8	10.3	0.56	0.615	-	-
Feed consumption (g/kid)	847.1	865.7	832.5	794.6	19.46	0.090	<0.01	<0.01
2. week	712.7	706.7	712.0	642.9	36.01
4. week	775.9	873.0	811.0	766.8	29.83
6. week	1010.0	965.9	892.4	905.7	26.61
8. week	814.6	778.7	675.7	853.1	19.71
Feed conversion ratio	4.43	4.57	4.62	4.65	0.22	0.908	<0.01	0.038
2. week	2.66	2.67	2.92	3.85	0.32
4. week	4.33	5.76	4.39	4.72	0.57
6. week	4.75	7.32	5.46	4.55	0.70
8. week	4.76	4.34	5.49	4.19	0.73

¹ PF – PF: Male kids born to dams fed a diet containing protected fat throughout pregnancy; PF – FO: Male kids born to dams fed a diet containing protected fat in the first half of gestation and fish oil in the second half; FO – FO: Male kids born to dams fed a diet containing fish oil throughout gestation; FO – PF: Male kids born to dams fed a diet containing fish oil in the first half of gestation and protected fat in the second half.

² SEM: pooled standard error of the means

³The initial live weight was used as covariant.

Table. 5 Liver enzyme activities in sera of male kids born to dams receiving omega-3 fatty acids in their rations at different stages of gestation

	Maternal Nutrition (MN)¹								SEM²		P³
	PF-PF		PF-FO		FO-FO		FO-PF				MN		day		MN x Day
n	11		12		13		11
ALT (IU/dl)	19.3		18.3		20.7		19.4		0.90		0.337		<0.01		0.816
1. day	18.2		16.7		18.1		17.6		1.99
28. day	17.6		17.4		20.4		18.4		1.22
56. day	22.1		20.9		23.5		22.3		1.03
AST (IU/dl)	102.8ab		94.0b		119.3a		98.5ab		6.30		0.029		0.274		0.038
1. day	99.9		80.4		124.1		107.4		11.15
28. day	101.0		99.3		110.8		95.3		5.29
56.day	107.6		102.2		122.9		92.9		7.04
GGT (IU/dl)	54.4		59.1		62.6		52.6		3.85		0.225		<0.01		0.159
1. day	61.6		55.1		60.2		58.7		5.31
28. day	47.4		54.4		59.4		48.6		4.58
56. day	54.3		67.9		68.2		50.3		4.89
ALP (IU/dl)	219.8		247.9		217.8		234.6		26.43		0.840		<0.01		0.309
1. day	170.6		221.2		142.4		155.8		29.94
28. day	238.2		240.3		267.1		257.2		34.64
56. day	250.7		282.3		243.9		290.7		36.89
Glucose (g/dl)		47.7b		51.1ab		45.5b		62.3a		3.17		<0.01		<0.01		0.316
1. day		65.2		70.2		66.7		82.8		6.80
28. day		34.4		40.7		37.9		48.3		3.12
56. day		43.5		42.5		32.0		55.8		4.07
Total cholesterol (g/dl)		64.7		61.6		70.2		61.2		3.68		0.256		<0.01		0.608
1. day		46.5		45.1		52.9		50.0		3.76
28. day		70.4		63.9		76.6		64.0		5.10
56.day		77.2		75.7		81.0		69.5		55.51
Triglycerides (g/dl)		46.4		45.8		48.4		44.3		3.53		0.851		0.087		0.051
1. day		39.4		43.8		56.5		45.1		7.46
28. day		52.0		46.1		54.4		45.4		4.99
56. day		47.9		47.5		34.2		42.2		4.29
Total protein (g/dl)		5.57ab		5.39b		5.89a		5.53ab		0.12		0.038		<0.01		0.363
1. day		5.29		5.18		5.57		5.51		0.14
28.day		5.50		5.18		5.80		5.29		0.16
56.day		5.91		5.78		6.29		5.81		0.18
Albumin (g/dl)		2.48		2.43		2.57		2.55		0.05		0.224		<0.01		0.073
1.day		2.35		2.48		2.48		2.53		0.06
28. day		2.41		2.31		2.54		2.45		0.07
56.day		2.67		2.49		2.69		2.67		0.07
Globulin (g/dl)		3.08ab		2.91b		3.36a		2.98ab		0.10		0.023		<0.01		0.645
1. day		2.92		2.67		3.19		2.95		0.11
28. day		3.08		2.87		3.30		2.84		0.12
56. day		3.23		3.19		3.59		3.14		0.17
Calcium (g/dl)		10.6		10.4		10.5		10.4		0.14		0.760		<0.01		0.574
1.day		10.2		10.2		10.3		10.2		0.18
28.day		10.7		10.5		10.8		10.4		0.20
56. day		10.8		10.5		10.5		10.6		0.17
Magnesium (g/dl)		6.94		6.89		6.97		7.11		0.14		0.704		0.01		0.081
1. day		6.69		6.44		6.87		6.51		0.22
28. day		7.05		7.46		6.83		7.47		0.25
56. day		7.06		6.77		7.22		7.35		0.22

²SEM: pooled standard error of the means

Table 6. Slaughter and carcass characteristics of male kids born to dams receiving omega-3 fatty acids in their rations at different stages of gestation

	Maternal Nutrition (MN)^{1, 2}				SEM³	P⁴
	PF-PF	PF-FO	FO-FO	FO-PF	SEM³	P⁴
Slaughter weight (kg)	24.7	24.4	22.4	22.2	1.37	0.465
Carcass characteristics
Hot carcass weight (kg)	10.4ab	10.5ab	11.0a	9.86b	0.28	0.078
Cold carcass weight (kg)	10.1ab	10.2ab	10.7a	9.63b	0.27	0.084
Skin weight (g)	1421.5	1648.3	1597.3	1612.9	70.92	0.149
Set weight (g)	1155.6	1149.4	1051.5	1155.9	38.27	0.192
Heart weight (g)	19.5	115.7	113.0	106.3	7.88	0.712
Neck weight (g)	414.1	405.1	458.3	369.1	26.66	0.162
Flank weight (g)	722.5	757.5	734.1	653.1	43.37	0.396
Shoulder head (g)	291.5	277.6	302.3	303.4	22.31	0.846
Thigh weight (g)	1424.3	1569.1	1447.3	1258.9	188.71	0.722
Arm weight (g)	1049.5	1055.9	1065.6	1009.4	39.53	0.756
lumbar weight (g)	861.1	827.2	883.3	770.9	37.81	0.205
Kidney weight (g)	114.9	134.4	154.4	134.1	23.64	0.704
Meat quality characteristics
Shear force	14.4	15.3	15.1	16.0	0.67	0.452
Hardness	5.81	5.41	6.02	5.55	0.21	0.217
Juiciness	15.6	16.1	14.9	13.7	0.71	0.174
pH	5.80	5.82	5.94	6.08	0.113	0.367

¹PF – PF: Male kids of dams fed a diet containing protected fat throughout pregnancy; PF – FO: Male kids of dams fed a diet containing protected fat in the first half of gestation and fish oil in the second half; FO – FO: Male kids of dams fed a diet containing fish oil throughout gestation;; FO – PF: Male kids of dams fed a diet containing fish oil in the first half of gestation and protected fat in the second half^.² Five kids were slaughtered from each group.

³SEM: pooled standard error of the means

⁴Slaughterweight was used as covariant.

Table 7. Fatty acid profile in M. longissimus dorsi of male kids born to dams receiving omega-3 fatty acids in their rations at different stages of gestation (g/100 g)

	Maternal Nutrition (MN)^{1, 2}				SEM³	P⁴
	PF-PF	PF-FO	FO-FO	FO-PF	SEM³	P⁴
Saturated fatty acid
Lauric acid (C12:0)	0.188	0.240	0.272	0.252	0.024	0.147
Myristic acid (C14:0)	2.72	3.07	3.21	3.13	0.21	0.429
Palmitic acid (C16:0)	23.3	24.2	24.6	23.9	0.62	0.541
Heptadecanoic acid (C17:0)	1.22	1.08	0.94	1.19	0.08	0.089
Stearic acid (C18:0)	18.3	17.0	19.0	16.2	0.96	0.190
Eicosanoic acid (C20:0)	0.87	0.86	1.11	0.75	0.108	0.160
Monounsaturated fatty acids
Palmitoleic acid (C16 :1)	1.63	1.85	1.56	1.84	0.12	0.230
Heptadecenoic acid (cis 10, C17:1)	0.67	0.68	0.48	0.73	0.07	0.097
Oleic acid (C18 : 1 n-9)	32.9b	36.0a	32.4b	34.9ab	0.86	0.029
Vaccenic acid (C18:1n7)	1.35	1.05	1.21	1.35	0.099	0.130
Erucic acid (C22:1n9)	1.38	0.84	0.73	0.68	0.185	0.072
Polyunsaturated fatty acids
Linoleic acid (C18:2n6)	6.18	4.76	4.82	4.88	0.43	0.100
Docosahexaenoic Acid (C22:6n3)	0.19a	0.11b	0.12b	0.09b	0.020	0.022
Total saturated fatty acid	46.6	46.4	49.1	45.5	1.03	0.113
Total monounsaturated fatty acids	37.9ab	40.4a	36.4b	39.5a	0.87	0.024
Total polyunsaturated fatty acids	6.37a	4.87b	4.94b	4.97b	0.45	0.090

² Five kids were slaughtered from each group.

³ SEM: pooled standard error of the means

⁴Slaughter weight was used as covariant.

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Editorial decision: Major revision with re-assessment
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The effects of omega-3 fatty acid used maternal rations during pregnancy on the fattening performances of male kids

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Journal Publication

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Abstract

Figures

Introduction

Material And Method

Determination of Live Weight and Live Weight Changes

Determination of Feed Consumption and Feed Conversion Efficiency

Determination of Biochemical Parameters

Collection of Data Related to Carcass and Meat Quality

Analysis of Fatty Acid Profile in Meats

Nutrient Analysis of the Feeds Used in the Experiment

Statistical Analysis

Results

Fattening Performance of Male Kids

Discussion

Conclusions

Declarations

References

Tables

Status:

Journal Publication

Version 1