http://dx.doi.org/10.4314/sajas.v54i3.11

 

High dietary inclusion of marula seed cake induces detrimental effects on performance, visceromorphometry, and immuno-physiology of broiler chickens

 

 

M.S. Mthana^I; D.M.N. Mthiyane^{I, II,} ; D.C. Onwudiwe^{III, IV}; M. Mwanza^{II, V}

^IDepartment of Animal Science, School of Agricultural Sciences, Faculty of Natural and Agricultural Sciences, North-West University (Mahikeng Campus), Private Bag X2046, Mmabatho 2735, South Africa
^IIFood Security and Safety Focus Area, Faculty of Natural and Agricultural Sciences, North-West University (Mahikeng Campus), Mmabatho, South Africa
^IIIMaterial Science Innovation and Modelling (MaSIM) Research Focus Area, Faculty of Natural and Agricultural Sciences, North-West University (Mahikeng Campus), Mmabatho, South Africa
^IVDepartment of Chemistry, School of Physical and Chemical Sciences, Faculty of Natural and Agricultural Sciences, North-West University (Mahikeng Campus), Mmabatho, South Africa
^VDepartment of Animal Health, School of Agricultural Sciences, Faculty of Natural and Agricultural Sciences, North-West University (Mahikeng Campus), Mmabatho, South Africa

 

 

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ABSTRACT

This study investigated the effects of incremental dietary levels of marula seed cake (MSC) in partial replacement of soyabean meal (SBM) and maize on growth performance, viscera macromorphometry, carcass traits, and haemato-biochemistry of broiler chickens during the starter, grower, and finisher phases. In a completely randomized design, 400 day-old Ross 308 broilers were randomly allocated to five diets with 0, 5, 10, 15, and 20% MSC, each with eight replicates of 10 (five of each sex). Weekly feed intake (FI), body weight gain (BWG), and feed conversion efficiency (FCE) were calculated; haemato-biochemistry was measured at day 42. FI was quadratically decreased by dietary MSC, of which the optimum inclusion was 150 g/kg, as BWG and FCE were linearly decreased by the marula by-product. MSC linearly decreased bird slaughter weight and hot and cold carcass weight. White blood cells, lymphocytes, and symmetric dimethylarginine decreased linearly but serum cholesterol concentrations increased linearly. Dietary inclusion of MSC at levels >150 g/kg induced detrimental effects on productive performance, visceral organs and development, carcass traits, and haemato-biochemistry of broiler chickens. There is therefore a need for strategies to resolve antinutritional effects of high dietary MSC to optimize its inclusion in broiler diets.

Keywords: poultry, marula seed cake, nutritional status, oleic acid, health

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Introduction

Soyabean meal (SBM) is the most preferred protein source for broiler diets in sub-Saharan Africa (SSA) and elsewhere, consequent to its high crude protein (CP) content (400-550 g/kg DM) and well-balanced profile of highly digestible amino acids, in comparison with other oilseed grains (Kidd et al., 2004). Nevertheless, the use of SBM in animal feeding is both economically and environmentally unsustainable. Large-scale soyabean cultivation incurs high variable costs and results in deforestation, biodiversity loss, climate change, pollution, coastal and riverine eutrophication, and acidification and worsens feed-food competition (Fearnside, 2001). Maize has predominantly been used as a source of energy for broiler diets, but this has increased the feed-food competition and feed costs (Okarter & Liu, 2010; Odo & Nnadi, 2013). Against this background, there is an urgent need for the investigation of alternative protein and energy-rich feed resources that are not only easily accessible and abundantly available, particularly to resource-limited smallholder farmers, but the production of which should be non-destructive to the environment. An example of such a feed is marula seed cake (MSC).

Marula (Sclerocarya birrea subsp. caffra) seed cake (MSC) is an industrial by-product that remains after oil extraction from the seed kernels of fruits fallen from marula trees that are indigenous and abundantly available throughout most of SSA from Niger to South Africa (Hall et al., 2002; Chirwa & Akinnifesi, 2008; Mlambo et al., 2011a; Leakey et al., 2022). Considering predicted future increases in climate change-associated frequency and severity of droughts in SSA (Schulze et al., 2007; Jiménez et al., 2020), MSC is an ideal, alternative dietary protein and energy source for broiler and livestock diets instead of SBM, maize, and other protein and energy ingredients, as it is produced from marula trees that are moderately resistant to drought (Hamidou et al., 2014). This feed resource has recently aroused great research interest, mainly in southern Africa, due to its high CP (470 g/kg DM) (Mdziniso et al., 2016). The essential and non-essential amino acid content is similar to SBM (except for lysine) and there is a high content of residual oil rich in the n-9 monounsaturated fatty acid (MUFA), oleic acid (72-85%) (Mthiyane & Mhlanga, 2017; Malebana et al., 2018). The high residual oil content (289.6 to 343.5 g/kg DM) (Mdziniso et al., 2016; Mthiyane & Mhlanga, 2017) render it an important energy source and potential replacer of maize and other energy-supplying ingredients in broiler diets. Previously, MSC was successfully used as an alternative protein source in the diet of beef cattle (Mlambo et al., 2011a), dairy cattle (Mdziniso et al., 2016), goats (Mlambo et al., 2011b), Japanese quails (Mazizi et al., 2020), and pigs (Mabena et al., 2022; Thabethe et al., 2022).

To the best of our knowledge, only a few studies have attempted to investigate dietary effects of MSC in broiler chickens and these have investigated the utility of this novel by-product only at the grower and finisher phases (Mthiyane & Mhlanga, 2017; Manyeula et al., 2022). No studies have considered responses of the modern bird to dietary MSC during the starter phase when their digestive systems would be envisaged to be the most sensitive to a novel, plant-derived feedstuff. Whilst Manyeula et al. (2022) studied this protein-rich by-product in broiler chickens, they measured only limited haematological and serum biochemical responses of the birds. As far as we are aware, there are currently no studies that have investigated dietary effects of MSC on the full repertoire of haematological and serum biochemical parameters, including immuno-physiological biomarkers of the meat-producing birds. Therefore, this study tested the hypothesis that partial dietary replacement of SBM and maize with MSC as a protein and energy source would maintain similar growth performance, visceral organs, carcass traits, haematology, and serum biochemistry responses of broiler chickens over the full production cycle (1 -42 d). The objective was therefore to investigate the effects of incremental dietary levels of MSC on growth performance, internal organs, carcass traits, and haemato-biochemical parameters of broiler chickens for the whole production cycle (1 -42 d).

 

Materials and Methods

The rearing and slaughter of broiler chickens used in this study was approved by the North-West University (NWU) Animal Production Sciences Research Ethics Committee (Approval #: NWU-00806-22-A5). The study was conducted at NWU Molelwane Experimental Farm during the summer season (October-November 2022). The farm is located (GPS coordinates: 25°40.459' S, 26°10.563 'E) outside Mahikeng City in the Mahikeng Local Municipality in Ngaka Modiri Molema District, North-West province of South Africa.

Yellow maize, SBM, and all other dietary ingredients (except MSC) were purchased from Simplegrow Agric Services (Pty) Ltd (Centurion, South Africa) whereas MSC was obtained from The Marula Company in Phalaborwa, Limpopo Province, South Africa. Upon arrival, 100 g of the by-product and experimental diets (Table 1) were milled using a laboratory mill (screen size: 1 mm) and stored in sealed, labelled polyethylene bags at room temperature (20-25 °C) for chemical analysis. Samples were then analysed for dry matter (DM) (method 930.15), ash (method 942.05), ether extract (EE) (method 920.39), CP (method 954.01), minerals (calcium and phosphorus) (method 991.25), and amino acids (lysine, methionine, and threonine) (method 982.30), following the guidelines of the AOAC (2005). Neutral detergent fibre (NDF), acid detergent fibre (ADF), and acid detergent lignin (ADL) were analysed following the procedures of van Soest et al. (1991). Condensed tannins (as leucocyanidin equivalents) were analysed according to the method described by Makkar (2000).

Five iso-caloric-nitrogenous diets were formulated such that they contained incremental levels (0, 5, 10, 15, and 20%) of MSC to partially replace SBM and maize to meet the nutritional requirements of broiler chickens at starter (d1 -14), grower (d15-28), and finisher (d29-42) phases (Table 1) (NRC, 1994). In a completely randomised design, 400 day-old Ross 308 broiler chicks with an average initial weight of 45.61 ± 0.67 g were randomly allocated to the dietary treatments, each with eight replicate pens (size = 1.8m high χ 1.5m long χ 1.5m wide) of 10 birds. Each pen had five males and five females. The experiment was carried out in a deep litter system in an environmentally-controlled broiler house where the temperature was maintained within 18 and 21 °C. The broiler house had semi-automatic curtains that were opened during the day (08:00 to 17:00) to allow natural light and closed in the evenings/night until the next morning (17:00 to 08:00). However, in week 1, artificial light was provided 24 h a day using electric lights in addition to infra-red lamps (one per pen) for brooding. Thereafter, infra-red lamps were removed, and electric lighting was only provided for 12 h (18:00 to 06:00) a day until the end of the experiment. Each pen had one feeder and one drinker. On placement, chicks were offered StressPack, which provided vitamins and electrolytes for the first 48 h. Fresh feed and water were offered ad libitum throughout the feeding trial. All pens were checked daily for mortalities, and dead birds were removed and recorded.

Following measurement of initial live weights upon arrival, broiler chickens were weighed weekly between 08:00 and 10:00 throughout the feeding trial by weighing all the birds in each pen until week 6. The weekly body weights, daily amounts of feed offered, and leftovers were recorded. Then BWG (g/bird/week) was calculated by subtracting the previous weekly body weight (g) from the current body weight (g), divided by the number of broilers per pen. Daily FI (g/bird/day) was calculated by subtracting the weight (g) of the leftover feed from the weight (g) of feed offered, divided by the number of birds per pen. The daily FI values were then converted into weekly averages of FI (g/bird/week) by combining pen averages over 7 d; FCE was calculated by dividing the weekly BWG by the weekly FI.

A day before slaughter (day 42), blood samples for haematology and serum biochemistry analysis were collected from 16 birds per treatment (two birds per pen) in the morning under veterinary supervision. Blood was collected from the wing vein with a 21-gauge needle and placed into purple-top, EDTA-coated vacutainer tubes for haematological analysis using an automated IDEXX LaserCyte Haematology Analyzer (IDEXX Laboratories (Pty) Ltd, Johannesburg, South Africa). The heterophil-to-lymphocyte ratio was calculated as heterophil divided by the lymphocyte values. For serum biochemistry analysis, blood samples were collected into red top Vacuette® Serum Clot Activator tubes without EDTA (Greiner Bio-One, GmbH, Frickenhausen, Germany). Serum biochemical parameters were analysed using an automated IDEXX Vet Test Chemistry Analyzer (IDEXX Laboratories (Pty) Ltd, Johannesburg, South Africa).

On the evening of day 42, six birds per pen (three males: three females) were fasted for 12 h (18:00 to 06:00) but provided with clean drinking water ad libitum. Next morning after group-weighing per pen to obtain the final live (slaughter) weights, birds were transported to Rooigrond poultry abattoir, ~30 km from the NWU experimental site. An hour after arrival at the abattoir, they were sacrificed humanely by cervical dislocation after electrical stunning (70 volts). The jugular vein was cut with a sharp knife at the base of the throat and allowed to bleed for 5 min. Following thorough bleeding, feathers were un-plucked, and the carcasses washed. The heads, necks, and feet were removed. Visceral organs were also removed by hand through an opening from the vent to the sternum and weighed individually. Hot carcass weight (HCW) was recorded immediately after slaughter at the abattoir, whereas cold carcass weight (CCW) was recorded 24 h post chilling (4 °C). Subsequently, chilling loss was calculated and expressed as a percentage using the formula:

Carcass cuts (breast, wing, thigh, and drumstick) were then removed by cutting from the joints of the carcass and through the shoulder area to remove the backbone from the breast. The internal organs and carcass cuts were then weighed and expressed as percentages of the HCW.

Weekly FI, BWG, and FCE data were analysed as repeated measures in SAS (2012) using the statistical model:

where yv_ijk = response variable, μ = overall mean, α = effect of diet, β; = effect of week, (aß)_ij = diet × week interaction effect, and ε_ijk = random error.

Overall FI, BWG, and FCE as well as data on haemato-biochemistry, internal organs, and carcass characteristics were analysed following the general linear model (GLM) procedure using the statistical model:

where y_ij = response variable, μ = overall mean, α_i = effect of diet, and +ε_ij = random error. The least square means (LSMeans) were compared using the probability of difference (PDIFF) option in the LSMeans statement and differences among them were deemed significant at P < 0.05.

Thereafter, the response surface regression (PROC RSREG) analysis was performed to estimate the optimum inclusion level of MSC according to the quadratic model:

where y = response variable; a and b = coefficients of the quadratic equation; c = intercept; x = MSC level (g/kg); and -b/2a = x value for optimal response.

 

Results and Discussion

The proximate composition of MSC is shown in Table 2. MSC contains high CP (471.8 g/kg DM) and OM contents, with low levels of EE, ash, fibre (NDF, ADF, and ADL) and CTs. In keeping with previous studies (Mdziniso et al., 2016; Mthiyane & Mhlanga, 2017), our results found MSC to have a similar CP content as SBM. Considering an amino acid composition similar to that of SBM, except for lysine (Malebana et al., 2018; Mthiyane & Mhlanga, 2017), MSC offers potential to replace SBM in poultry diets in southern Africa and elsewhere. Local marula oil-extracting factories have improved their efficiency of oil extraction from marula kernels, as evidenced by the relatively low residual oil content of MSC used in this study compared to previous MSC products (289.6-343.5 g/kg DM) (Mdziniso et al., 2016; Mthiyane & Mhlanga, 2017). With more improvements in oil extraction efficiency, iso-energetic MSC-containing broiler and livestock diets can henceforth be formulated with greater ease and the feed product is expected to have less problems with fungal and hence mycotoxin infestation, as observed previously (Mthiyane & Mhlanga, 2017).

 

 

Of interest also is the relatively low fibre content in MSC used in this study in comparison to values observed in previous studies (Hlongwana et al., 2021; Mabena et al., 2022). The observed low fibre content of MSC renders this by-product even more ideal for use in diets of broiler chickens and other non-ruminants that are unable to utilize high fibre-containing diets (Zijlstra et al., 2012; Jiménez-Moreno & Mateos, 2013). The current study showed MSC to be richer in ash, an indicator of the mineral content, compared to previous MSC by-products (48.5-54.3 g/kg DM) (Mthiyane & Mhlanga, 2017; Hlongwana et al., 2021; Mabena et al., 2022). The concentration of condensed tannins in MSC used in this study is higher than that reported by Malebana et al. (2018) yet within the normal range considered safe for the by-product to be used in broiler diets without induction of adverse effects on bird growth (Hidayat et al., 2021). Previous studies have shown that inclusion of up to 3% tannins in broiler diets improves gut health and digestive performance (Tandiang et al., 2014; Huang et al., 2018).

Table 3 shows the effects of incremental levels of MSC on weekly and overall FI, BWG, and FCE, as well as mortality of birds. Repeated measures analysis revealed a significant diet × week interaction on weekly BWG (P <0.05) but not FI (P >0.05) and FCE (P >0.05). Regarding FI, dietary MSC induced a linear decrease (P <0.01) in this parameter in week 1, a quadratic decrease in weeks 2 (P <0.05), 3 (P <0.01), and 4 (P = 0.001), as well as a linear decrease in week 5 (P <0.01). There was no effect (P >0.05) of dietary MSC inclusion on FI in week 6. Overall, FI was quadratically decreased (P <0.01) by dietary inclusion of incremental levels of MSC. In terms of FI, the optimum dietary inclusion level of the marula by-product was 150 g/kg, beyond which there was a sharp decrease in this parameter.

Dietary inclusion of MSC induced a linear decrease in BWG in weeks 1 (P = 0.001) and 3 (P <0.01), a quadratic decrease in week 4 (P = 0.001), and a linear decrease in week 5 (P <0.01). However, there was no effect (P >0.05) of dietary MSC on BWG in weeks 2 and 6. Overall, BWG was linearly decreased (P = 0.001) by dietary inclusion of increasing levels of MSC, with the optimum inclusion level, in terms of this parameter, of 100 g/kg, beyond which BWG decreased.

Inclusion of dietary incremental levels of MSC linearly decreased FCE in broilers in weeks 1 (P <0.01), 3 (P <0.01), and 5 (P <0.01), whereas FCE decreased quadratically from week 4 (P <0.01). Similar to BWG, there was no effect (P >0.05) of dietary MSC on FCE in weeks 2 and 6. Overall, FCE decreased linearly (P <0.01) with increasing dietary levels of MSC in broiler diets, with the optimum inclusion level of the marula by-product, in terms of this parameter, found to be 100 g/kg, beyond which FCE decreased. The results also indicated no effect (P >0.05) of dietary MSC on all performance parameters (FI, BWG, and FI) in broiler chickens during week 6 of the study. Similarly, mortality was not affected (P >0.05) by dietary MSC (Table 3).

As part of the investigation of the nutritive value of MSC for broiler chickens, this study tested effects of incremental dietary inclusion of the marula oil extraction by-product on broiler growth performance and mortality during the whole production cycle from d1 to 42. The observed increase in FI from 0 to 150 g/kg, as well as BWG and FCE from 0 to 100 g/kg of dietary MSC inclusion level beyond which they decreased, corroborates previous observations in pig studies by Thabethe et al. (2020), Hlongwana et al. (2021), and Mabena et al. (2022) but contradicts those of Mazizi et al. (2019) in Japanese quails. In a previous study, the decrease in performance parameters with increasing inclusion levels of MSC was suspected to be induced by extensive lipid peroxidation and mycotoxin infestation of MSC (Mthiyane & Mhlanga, 2017); these researchers found high lipid peroxidation and low concentrations of mycotoxins deoxynivalenol (DON) and T-2 toxin in MSC.

Notwithstanding, there is a possibility that the observed decrease in performance at high (150 to 200 g/kg) dietary MSC inclusion levels may also be related to the high oleic acid content in the residual oil-rich MSC. Dietary oleic acid was previously shown to decrease food intake through induction of satiety in mice (Igarashi et al., 2022) and to decrease food energy intakes in humans (Mennella et al., 2015) by eliciting the production of oleoylethanolamide (Schwartz et al., 2008). Oleoylethanolamide is known to decrease food intake (Rodriguez de Fonseca et al., 2001; Fu et al., 2003; Piomelli, 2013) through a mechanism involving the histaminergic system (Provensi et al., 2014). Oleic acid has the capacity to regulate body weight in animals, as was demonstrated through a decrease in this parameter in rats fed a diet supplemented with 100 g/kg olive oil (Nogoy et al., 2020), a rich source of oleic acid (70-80%). Mechanistically, this might occur via high MUFA diets exhibiting greater rates of oxidation, leading to decreased body weight (Liu et al., 2016). Another putative mechanism might involve oleic acid inducement of a laxative (cathartic) effect, as has been demonstrated in rats (Beubler & Juan, 1979). These effects of oleic acid may therefore explain the decreased FI, BWG, and FCE in broiler chickens fed high dietary levels of MSC in the current study. These mechanisms may also explain the observed decrease in slaughter weight, HCW, and CCW in these broilers when fed high (150-200 g/kg) dietary inclusion levels of MSC.

The internal organs and carcass traits of broiler chickens fed diets supplemented with varying inclusion levels of MSC are shown in Tables 4 and 5. There were neither linear nor quadratic effects ( P >0.05) of MSC on the weights and lengths of all internal organs (Table 5). Similarly, there were neither linear nor quadratic effects (P >0.05) of MSC on all carcass traits, except for the SW, HCW, and CCW (Table 5). In this regard, we observed linear decreases in SW (P = 0.001), HCW (P = 0.001), and CCW (P = 0.001) of broilers in response to increasing dietary inclusion levels of MSC.

Considering the lack of effect of dietary MSC on the weights and lengths of all visceral organs, it would therefore appear that this alternative feed resource does not contain detrimental antinutritional factors and is thus safe to incorporate at 50 to 100 g/kg inclusion levels in broiler chicken diets. This notion is further supported by the lack of effect of dietary MSC on mortality in this study. Generally, the feeding of alternative, plant-derived feedstuffs or their extracts with high levels of antinutritional factors and fibre is associated with increased size of the digestive tract (Jørgensen et al., 1996; Egbu et al., 2022). Further, the lack of effect of dietary MSC on all performance parameters even at high inclusion levels of MSC (200 g/kg) in week 6 suggests age-dependent attainment of adaptation to consumption of the novel, alternative protein source in broiler chickens. This was reflected in the significant diet χ week interaction effect on weekly BWG. The digestive system of broiler chickens undergoes major anatomical and physiological changes as the birds grow, with increases in size and length, as well as the ability to secrete digestive enzymes with concomitant improved digestive ability, as they grow older (Ravindran & Abdollahi, 2021). If MSC contained any antinutritional substances, their adverse impact appears to have decreased as the age of birds advanced, similarly to previous observations (Rao et al., 2013; Erdaw et al., 2017).

The haematological responses of broiler chickens to graded dietary levels of MSC are shown in Table 6. The results demonstrated no effects (P >0.05) of MSC inclusion on all haematological parameters, except for white blood cells and lymphocytes. In this regard, MSC linearly decreased white blood cells (P <0.01) and lymphocytes (P <0.05) of birds. The lack of effect of dietary MSC inclusion on most haematological parameters of the modern birds in this study is also indicative of reasonable biosafety of the by-product in relation to the health of the birds.

The kernels of marula fruits are a safe and delicious source of nutrition generally enjoyed by millions of predominantly rural people in numerous countries in Africa without any health perturbations. Generally, they are consumed as a snack (Mashau et al., 2022), incorporated into porridge and boiled meat as flavour enhancers (Petje, 2009), or their extracted oil is used for meat preservation (Duke, 1989; Maroyi, 2013). In poultry nutrition, their dietary consumption in the form of MSC has also elicited no deleterious effects in Japanese quails (Mazizi et al., 2019). Hence, their detrimental effects on broiler chicken white blood cells and lymphocytes at dietary inclusion levels beyond 100 g/kg as observed in the current study was unexpected. Notwithstanding, some studies have reported inhibitory effects of oleic acid in its neat form (Menendez et al., 2005; Carrillo et al., 2011 ; Hidalgo et al., 2011) or as dietary olive oil (Verlengia et al., 2003; Llado et al., 2010) or cashew kernel oil (Yaqoob et al., 1995) on lymphocytes and their proliferation in different tissues, including blood.

Consumption of the oleic acid-rich Mediterranean diet decreases the number of leukocytes and platelets in human subjects (Ambring et al., 2016). The mechanism underlying these deleterious effects of oleic acid on leukocytes, including lymphocytes, may involve the MUFA-induced cellular oxidative stress, mitochondrial depolarization (Cury-Boaventura et al., 2004, 2005 & 2006; Ambring et al., 2016) and apoptosis (Jeffery et al., 1996 & 1997). The current study is the first to investigate the full repertoire of haematology in broiler chickens. Hence, it remains to be seen in future studies whether diets supplemented with high levels of MSC would induce similar deleterious effects on leukocytes in other breeds of chicken. The molecular mechanisms underlying the observed MSC-induced perturbations in immunological parameters of broilers and other chicken breeds need to be elucidated.

The effects of dietary incorporation of graded levels of MSC on serum biochemical parameters of broiler chickens are shown in Table 7. Results showed no effect (P >0.05) of MSC on all serum biochemistry parameters, except for symmetric dimethylarginine (SDMA) and cholesterol. In this respect, dietary MSC linearly decreased (P <0.01) serum SDMA concentrations as the MSC level increased from 0 to 150 g/kg, beyond which it increased with 150 to 200 g/kg MSC. In contrast, serum cholesterol showed a linear increase (P = 0.001) to increasing dietary inclusion levels of MSC.

The safety of MSC as broiler chicken feed at low (50-150 g/kg) and its apparent toxicity at high (200 g/kg) dietary inclusion levels was clearly represented in the SDMA responses. Strongly correlated with renal function, SDMA is a biomarker of acute kidney injury (Kielstein et al., 2006) and has previously been measured in broiler and quail studies of alternative protein sources and phytogenic feed additives (Marareni & Mnisi, 2020; Matshogo et al., 2021). Considering the linearly decreasing serum SDMA concentrations in broilers fed diets with 0-150 g/kg MSC, it is evident that MSC is safe to use at these relatively low dietary inclusion levels but induced kidney injury in the chickens when it was included at a higher (200 g/kg) content, mirroring the observed decremental responses in performance and immunological parameters of birds fed diets with such high dietary inclusion levels of the marula oil extraction by-product.

As mentioned above, it is argued that the high oleic acid content of MSC, particularly at 200 g/kg inclusion of the alternative feed resource, induced cellular oxidative stress (Cury-Boaventura et al., 2004, 2005, 2006) and possibly apoptosis (Jeffery et al., 1996 & 1997) in the chickens. Lending support to this contention are previous observations of elevated SDMA levels in disease conditions involving oxidative stress, including diabetes mellitus, atherosclerosis, inflammation, apoptosis, and compromised immune function (Tain & Hsu, 2017). Some studies have postulated that SDMA itself may be an inducer of oxidative stress by elevating reactive oxygen species in monocytes (Schepers et al., 2009) whilst enhancing NADPH-oxidase through endothelial Toll-like receptor-2 activation (Speer et al., 2013). Evidence reporting abrogative effects of antioxidants, including epigal-locatechin-3-gallate, melatonin, N-acetylcysteine, vitamin E on kidney injury, measured as asymmetric dimethylarginine (ADMA), a structural isomer of SDMA (Tain & Hsu, 2017) further reinforces the contention that oleic acid is pro-oxidative in broiler chickens at high dietary MSC inclusion levels. The current study is the first to investigate SDMA responses to dietary MSC supplementation in broiler chickens and thus there are currently no comparable values in the scientific literature. In future studies, there is a need to investigate biomarkers of and mechanisms underlying oxidative stress in birds fed high MSC-containing diets.

The linear increase in broiler serum cholesterol responses to incremental dietary inclusion levels of MSC was interesting. Whilst our serum cholesterol values were ~1.8 times lower than plasma cholesterol values previously observed in quails (Mazizi et al., 2022), there are currently no comparable literature serum cholesterol responses to dietary MSC supplementation in broilers. However, it is evident that the observed increase in the chicken serum cholesterol concentrations with increasing dietary MSC inclusion levels in the current study is associated with oleic acid. A previous study reported that the consumption of oleic acid-rich olive oil increased blood plasma and adipose tissue concentrations of high-density lipoprotein cholesterol (HDL-C) (Nogoy et al., 2020). Apparently, the MUFA has the unique ability to selectively increase the content of the health-beneficial blood HDL-C, whilst decreasing that of its cardiovascular disease (CVD)-associated, low-density lipoprotein cholesterol (LDL-C) counterpart (Rudel et al., 1995; Kwon & Choi, 2015; Nogoy et al., 2020), resulting in the attenuation of CVD risk in patients with hypercholesterolaemia (Zambón et al., 2000; Bemelmans et al., 2002). Hence, it will be necessary to measure concentrations of both HDL-C and LDL-C in MSC-fed broilers in future studies to discern which of the two cholesterol moieties is responsible for the observed elevation in serum cholesterol levels of birds fed incremental marula by-product-containing diets. The observed dietary MSC-associated increase in broiler serum cholesterol suggests a need for investigation of underlying molecular mechanisms in terms of cholesterol biosynthesis in future studies.

 

Conclusion

Up to 150 g/kg of MSC can be incorporated in broiler chicken diets to substitute SBM without adverse effects on growth performance, visceral organ sizes, carcass yield, and immuno-physiology of birds. There is a need for strategies to resolve antinutritional effects of high dietary levels of MSC to optimize its inclusion in broiler diets so as to completely replace SBM.

 

Acknowledgement

The first author acknowledges the PhD Scholarship from the National Research Foundation (NRF) (Grant no: 141668) and North-West University Postgraduate Bursary. Financial support from the NWU School of Agricultural Sciences and Department of Animal Science is greatly acknowledged.

Author Contributions

MSM conceptualised the study, collected the data, conducted the statistical analyses, interpreted the results, and wrote the initial draft of this manuscript; DMNM conceptualised the study, developed the original hypotheses, was involved in supervision, collaborated in the interpretation of results, and finalised the manuscript; dCo was involved in supervision, collaborated in the interpretation of results, and finalised the manuscript; MM was also involved in supervision, collaborated in the interpretation of results, and finalised the manuscript.

Conflict of Interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript; or in the decision to publish the results.

 

References

Ambring, A., Johansson, M., Axelsen, M., Gan, L., Strandvik, B. & Friberg, P., 2006. Mediterranean-inspired diet lowers the ratio of serum phospholipid n-6 to n-3 fatty acids, the number of leukocytes and platelets, and vascular endothelial growth factor in healthy subjects. Amer. J. Clin. Nutr. 83(3), 575-581. https://doi.org/10.1093/ajcn.83.3.575.         [ Links ]

AOAC., 2005. Official methods of analysis of AOAC (16^th edition ed). Association of Analytical Communities.         [ Links ]

Bemelmans, W.J., Broer, J., Feskens, E.J., Smit, A.J., Muskiet, F.A., Lefrandt, J.D., Bom, V.J., May, J.F. & Meyboom-de Jong, B., 2002. Effect of an increased intake of α-linolenic acid and group nutritional education on cardiovascular risk factors: the Mediterranean Alpha-linolenic Enriched Groningen Dietary Intervention (MARGARIN) study. Amer. J. Clin. Nutr. 75(2), 221 -227. https://doi.org/10.1093/ajcn/75.2.221.         [ Links ]

Beubler, E. & Juan, H., 1979. Effect of ricinoleic acid and other laxatives on net water flux and prostaglandin E release by the rat colon. J. Pharm. Pharmacol. 31(1), 681-685. https://doi.org/10.1111/j.2042-7158.1979.tb13628.x.         [ Links ]

Carrillo, C., del Mar Cavia, M., Roelofs, H., Wanten, G. & Alonso-Torre, S.R., 2011. Activation of human neutrophils by oleic acid involves the production of reactive oxygen species and a rise in cytosolic calcium concentration: A comparison with N-6 polyunsaturated fatty acids. Cell Physiol. Biochem. 28(2), 329-338. https://doi.org/10.1159/000331749.         [ Links ]

Chirwa, P. & Akinnifesi, F., 2008. Ecology and biology of Uapaca kirkiana, Strychnos cocculoides and Sclerocarya birrea in Southern Africa. In Indigenous fruit trees in the tropics: domestication, utilization and commercialization (pp. 322-340). CABI Wallingford UK. https://doi.org/10.1079/9781845931100.0322.         [ Links ]

Cury-Boaventura, M.F., Kanunfre, C. C., Gorjão, R., de Lima, T.M. & Curi, R., 2006. Mechanisms involved in Jurkat cell death induced by oleic and linoleic acids. Clin. Nutr. 25(6), 1004-1014. https://doi.org/10.1016/j.clnu.2006.05.008.         [ Links ]

Cury-Boaventura, M.F., Pompéia, C. & Curi, R., 2004. Comparative toxicity of oleic acid and linoleic acid on Jurkat cells. Clin. Nutr. 23(4), 721-732. https://doi.org/10.1016/j.clnu.2003.12.004.         [ Links ]

Cury-Boaventura, M.F., Pompéia, C. & Curi, R., 2005. Comparative toxicity of oleic acid and linoleic acid on Raji cells. Nutrition. 21(3), 395-405. https://doi.org/10.1016/j.nut.2004.07.007.         [ Links ]

Duke, J.A. 1989. CRC Handbook of Nuts Boca Raton (Florida). In: CRC Press, Inc.         [ Links ]

Egbu, C.F., Motsei, L.E., Yusuf, A.O. & Mnisi, C.M., 2022. Effect of Moringa oleífera seed extract administered through drinking water on physiological responses, carcass and meat quality traits, and bone parameters in broiler chickens. Appl. Sci. 12(20), 10330. https://doi.org/10.3390/app122010330.         [ Links ]

Erdaw, M., Perez-Maldonado, R., Bhuiyan, M. & Iji, P., 2017. Partial replacement of commercial soybean meal with raw, full-fat soybean meal supplemented with varying levels of protease in diets of broiler chickens. S. Afr. J. Anim. Sci. 47(1), 61-71. http://dx.doi.org/10.4314/sajas.v47i1.10.         [ Links ]

Fearnside, P.M. 2001. Soybean cultivation as a threat to the environment in Brazil. Environ. Conserv. 28(1), 23-38. https://doi.org/10.1017/S0376892901000030.         [ Links ]

Fu, J., Gaetani, S., Oveisi, F., Lo Verme, J., Serrano, A., Rodríguez de Fonseca, F., Rosengarth, A., Luecke, H., Di Giacomo, B. & Tarzia, G., 2003. Oleoylethanolamide regulates feeding and body weight through activation of the nuclear receptor PPAR-α. Nature. 425(6953), 90-93. https://doi.org/10.1038/nature01921.         [ Links ]

Hall, J., O'brien, E. & Sinclair, F., 2002. Sclerocarya birrea: A Monograph. School of Agriculture and Forest Science Publication No. 19. University of Wales, Bangor, UK, 157.         [ Links ]

Hamidou, A., Iro, D.G., Boubé, M., Malick, T.S. & Ali, M., 2014. Potential germination and initial growth of Sclerocarya birrea (A. Rich.) Hochst, in Niger. J. Appl. Biosci. 76, 6433-6443. https://doi.org/10.4314/jab.v76i1.12.         [ Links ]

Hidalgo, M.A., Nahuelpan, C., Manosalva, C., Jara, E., Carretta, M.D., Conejeros, I., Loaiza, A., Chihuailaf, R. & Burgos, R.A., 2011. Oleic acid induces intracellular calcium mobilization, MAPK phosphorylation, superoxide production and granule release in bovine neutrophils. Biochem. Biophys. Res. Comm. 409(2). 280-286. https://doi.org/10.1016/j.bbrc.2011.04.144.         [ Links ]

Hidayat, C., Irawan, A., Jayanegara, A., Sholikin, M.M., Prihambodo, T.R., Yanza, Y.R., Wina, E., Sadarman, S., Krisnan, R. & Isbandi, I., 2021. Effect of dietary tannins on the performance, lymphoid organ weight, and amino acid ileal digestibility of broiler chickens: A meta-analysis. Vet. World. 14(6), 1405. https://doi.org/10.14202%2Fvetworld.2021.1405-1411.         [ Links ]

Hlongwana, F., Thabethe, F., Thomas, R. & Chimonyo, M., 2021. Nitrogen balance in slow-growing Windsnyer pigs fed on incremental levels of amarula (Sclerocarya birrea subsp. caffra) nut cake. Trop. Anim. Health Prod. 53(3), 364. https://doi.org/10.1007/s11250-021-02808-x.         [ Links ]

Huang, Q., Liu, X., Zhao, G., Hu, T. & Wang, Y., 2018. Potential and challenges of tannins as an alternative to in-feed antibiotics for farm animal production. Anim. Nutr. 4(2), 137-150. https://doi.org/10.1016/j.aninu.2017.09.004.         [ Links ]

Igarashi, M., Iwasa, K., Hayakawa, T., Tsuduki, T., Kimura, I., Maruyama, K. & Yoshikawa, K., 2022. Dietary oleic acid contributes to the regulation of food intake through the synthesis of intestinal oleoylethanolamide. Front. Endocrinol. 13. https://doi.org/10.1016/j.plefa.2020.102228.         [ Links ]

Jeffery, N., Yaqoob, P., Newsholme, E. & Calder, P., 1996. The effects of olive oil upon rat serum lipid levels and lymphocyte functions appear to be due to oleic acid. Ann. Nutr. Metabol. 40(2), 71-80. https://doi.org/10.1159/000177898.         [ Links ]

Jeffery, N.M., Cortina, M., Newsholme, E.A. & Calder, P.C., 1997. Effects of variations in the proportions of saturated, monounsaturated, and polyunsaturated fatty acids in the rat diet on spleen lymphocyte functions. Brit. J. Nutr. 77(5), 805-823. https://doi.org/10.1079/bjn19970077.         [ Links ]

Jiménez, A., Saikia, P., Giné, R., Avello, P., Leten, J., Liss Lymer, B., Schneider, K. & Ward, R., 2020. Unpacking water governance: A framework for practitioners. Water. 12(3), 827. https://doi.org/10.3390/w12030827.         [ Links ]

Jiménez-Moreno, E. & Mateos, G.G., 2013. Use of dietary fibre in broilers. San Juan del Rio, Queretaro: In Memorias De La Sexta Reunión Anual Aecacem, 2013.         [ Links ]

Jørgensen, H., Zhao, X.Q., Knudsen, K.E.B. & Eggum, B.O., 1996. The influence of dietary fibre source and level on the development of the gastrointestinal tract, digestibility and energy metabolism in broiler chickens. Brit. J. Nutr. 75(3), 379-395. https://doi.org/10.1079/bjn19960141.         [ Links ]

Kidd, M., McDaniel, C., Branton, S., Miller, E., Boren, B. & Fancher, B., 2004. Increasing amino acid density improves live performance and carcass yields of commercial broilers. J. Appl. Poult. Res. 13(4), 593-604. https://doi.org/10.1093/japr/13.4.593.         [ Links ]

Kielstein, J.T., Salpeter, S.R., Bode-Boeger, S.M., Cooke, J.P. & Fliser, D., 2006. Symmetric dimethylarginine (SDMA) as endogenous marker of renal function - a meta-analysis. Nephrol. Dialys. Transplan, 21(9), 2446-2451. https://doi.org/10.1093/ndt/gfl292.         [ Links ]

Kwon, H.N. & Choi, C.B., 2015. Comparison of lipid content and monounsaturated fatty acid composition of beef by country of origin and marbling score. J. Korean. Soc. Food Sci. Nutr, 44(12), 1806-1812. http://dx.doi.org/10.3746/jkfn.2015.44.12.1806.         [ Links ]

Leakey, R.R., Tientcheu Avana, M.L., Awazi, N.P., Assogbadjo, A.E., Mabhaudhi, T., Hendre, P.S., Degrande, A., Hlahla, S. & Manda, L., 2022. The future of food: Domestication and commercialization of indigenous food crops in Africa over the third decade (2012-2021). Sustainability. 14(4), 2355. https://doi.org/10.3390/su14042355.         [ Links ]

Liu, X., Kris-Etherton, P.M., West, S.G., Lamarche, B., Jenkins, D.J., Fleming, J.A., McCrea, C.E., Pu, S., Couture, P. & Connelly, P.W., 2016. Effects of canola and high oleic acid canola oils on abdominal fat mass in individuals with central obesity. Obesity. 24(11), 2261-2268. https://doi.org/10.1002/oby.21584.         [ Links ]

Llado, V., Gutierrez, A., Martínez, J., Casas, J., Terés, S., Higuera, M., Galmés, A., Saus, C., Besalduch, J. & Busquets, X., 2010. Minerval induces apoptosis in Jurkat and other cancer cells. J. Cell Mol. Med. 14(3), 659-670. https://doi.org/10.1111%2Fj.1582-4934.2008.00625.x.         [ Links ]

Mabena, P., Ratsaka, M., Nkukwana, T., Malebana, I. & Nkosi, B., 2022. Growth performance, nutrient digestibility and carcass characteristics of pigs fed diets containing amarula (Sclerocarya birrea A. Rich) nut cake as replacement to soybean meal. Trop. Anim. Health Prod. 54(1), 8. https://doi.org/10.1007/s11250-021-03016-3.         [ Links ]

Makkar, H. 2000. Quantification of tannins in tree foliage. FAO/IAEA Working Document IAEA, Vienna.         [ Links ]

Malebana, I.M., Nkosi, B.D., Erlwanger, K.H. & Chivandi, E., 2018. A comparison of the proximate, fibre, mineral content, amino acid and the fatty acid profile of marula (Sclerocarya birrea caffra) nut and soyabean (Glycine max) meals. J. Sci. Food Agric. 98(4), 1381-1387. https://doi.org/10.1002/jsfa.8604.         [ Links ]

Manyeula, F., Loeto, O., Phalaagae, K., Baleseng, L., Sebolai, T., Molapisi, M., Khumoetsile, T. & Moreki, J., 2022. Morula (Sclerocarya birrea) kernel cake as a partial soybean meal replacer in Ross 308 broiler diets: Effects on feed utilisation, growth performance, and selected blood parameters. S. Afri. J. Anim. Sci. 52(6), 802-810. http://dx.doi.org/10.4314/sajas.v52i6.06.         [ Links ]

Marareni, M. & Mnisi, C.M., 2020. Growth performance, serum biochemistry and meat quality traits of Jumbo quails fed with mopane worm (Imbrasia belina) meal-containing diets. Vet. Anim. Sci. 10, 100141. https://doi.org/10.1016/j.vas.2020.100141.         [ Links ]

Maroyi, A. 2013. Traditional use of medicinal plants in south-central Zimbabwe: Review and perspectives. J. Ethnobiol. Ethnomed. 9(1), 1-18. https://doi.org/10.1186/1746-4269-9-31.         [ Links ]

Mashau, M.E., Kgatla, T.E., Makhado, M.V., Mikasi, M.S. & Ramashia, S.E., 2022. Nutritional composition, polyphenolic compounds, and biological activities of marula fruit (Sclerocarya birrea) with its potential food applications: A review. Int. J. Food Prop. 25(1), 1549-1575. https://doi.org/10.1080/10942912.2022.2064491.         [ Links ]

Matshogo, T.B., Mnisi, C.M. & Mlambo, V., 2021. Effect of pre-treating dietary green seaweed with proteolytic and fibrolytic enzymes on physiological and meat quality parameters of broiler chickens. Foods 10(8), 1862. https://doi.org/10.1016/j.livsci.2021.104652.         [ Links ]

Mazizi, B.E., Erlwanger, K.H. & Chivandi, E., 2020. The effect of dietary marula nut meal on the physical properties, proximate and fatty acid content of Japanese quail meat. Vet. Anim. Sci. 9, 100096. https://doi.org/10.1016/j.vas.2020.100096.         [ Links ]

Mazizi, B.E., Erlwanger, K.H. & Chivandi, E., 2022. Effect of dietary marula nut meal on liver lipid content and surrogate markers of liver and kidney function of broiler and layer Japanese quail. https://orcid.org/0000-0002-7408-488X.         [ Links ]

Mazizi, B.E., Moyo, D., Erlwanger, K.H. & Chivandi, E., 2019. Effects of dietary Sclerocarya birrea caffra (marula) nut meal on the growth performance and viscera macromorphometry of broiler Japanese quail. J. Appl. Poult. Res. 28(4), 1028-1038. https://doi.org/10.3382/japr/pfz064.         [ Links ]

Mdziniso, P., Dlamini, A., Khumalo, G. & Mupangwa, J., 2016. Nutritional evaluation of marula (Sclerocarya birrea) seed cake as a protein supplement in dairy meal. J. Appl. Life Sci. Int. 4(3), 1-11. http://dx.doi.org/10.9734/JALSI/2016/23273.         [ Links ]

Menendez, J., Vellon, L., Colomer, R. & Lupu, R., 2005. Oleic acid, the main monounsaturated fatty acid of olive oil, suppresses Her-2/neu (erbB-2) expression and synergistically enhances the growth inhibitory effects of trastuzumab (Herceptin™) in breast cancer cells with Her-2/neu oncogene amplification. Ann. Oncol. 16(3), 359-371. https://doi.org/10.1093/annonc/mdi090.         [ Links ]

Mennella, I., Savarese, M., Ferracane, R., Sacchi, R. & Vitaglione, P., 2015. Oleic acid content of a meal promotes oleoylethanolamide response and reduces subsequent energy intake in humans. Food Func. 6(1), 203-209. https://doi.org/10.1039/c4fo00697f.         [ Links ]

Mlambo, V., Dlamini, B., Ngwenya, M., Mhazo, N., Beyene, S. & Sikosana, J., 2011a. In sacco and in vivo evaluation of marula (Sclerocarya birrea) seed cake as a protein source in commercial cattle fattening diets. Livest. Res. Rural. Devel. 23(5), 1-10.         [ Links ]

Mlambo, V., Dlamini, B., Nkambule, M., Mhazo, N. & Sikosana, J., 2011b. Nutritional evaluation of marula (Sclerocarya birrea) seed cake as a protein supplement for goats fed grass hay. Trop. Agric. 41(3216), 010035-010009.         [ Links ]

Mthiyane, D.M.N. & Mhlanga, B.S., 2017. The nutritive value of marula (Sclerocarya birrea) seed cake for broiler chickens: nutritional composition, performance, carcass characteristics and oxidative and mycotoxin status. Trop. Anim. Health Prod. 49, 835-842. https://doi.org/10.1007%2Fs11250-017-1269-9.         [ Links ]

Nogoy, K. M.C., Kim, H. J., Lee, Y., Zhang, Y., Yu, J., Lee, D.H., Li, X.Z., Smith, S.B., Seong, H.A. & Choi, S.H., 2020. High dietary oleic acid in olive oil supplemented diet enhanced omega-3 fatty acid in blood plasma of rats. Food Sci. Nutr. 8(7), 3617-3625. https://doi.org/10.1002%2Ffsn3.1644.         [ Links ]

NRC. 1994. Nutrient Requirements of Poultry (9th ed.). National Academy Pres.         [ Links ]

Odo, B.I., Nnadi, A.E., 2013. Growth response of quails (Coturnix coturnix japonica) to varying levels of cassava tuber meal (Manihot esculenta) as replacement for maize (Zea mays). Rev. Cie. UDO Agric. 13, 146-149. http://dx.doi.org/10.9734/AJEA/2014/11412.         [ Links ]

Okarter, N. & Liu, H.R., 2010. Health benefits of whole grain phytochemicals. Crit. Rev. Food Sci. Nutr. 50 (3), 193-208. https://doi.org/10.1080/10408390802248734.         [ Links ]

Petje, K.F. 2009. Determination of fruit yield and fruit quality in marula (Sclerocaryabirrea subsp. caffra) selections. MSc Thesis: University of Pretoria, South Africa.         [ Links ]

Piomelli, D. 2013. A fatty gut feeling. Trends Endocrinol. Metabol. 24(7), 332-341. https://doi.org/10.1016/j.tem.2013.03.001.         [ Links ]

Provensi, G., Coccurello, R., Umehara, H., Munari, L., Giacovazzo, G., Galeotti, N., Nosi, D., Gaetani, S., Romano, A. & Moles, A., 2014. Satiety factor oleoylethanolamide recruits the brain histaminergic system to inhibit food intake. Proceed. Nat. Acad. Sci. 111(31), 11527-11532. https://doi.org/10.1073/pnas.1322016111.         [ Links ]

Rao, S., Prasad, K. & Rajendran, D., 2013. Recent advances in amelioration of anti-nutritional factors in livestock feedstuffs. Animal Nutrition and Reproductive Physiology (Recent Concepts). Satish Serial Publishing House, Delhi, India. pp 655-678.         [ Links ]

Ravindran, V. & Abdollahi, M.R., 2021. Nutrition and digestive physiology of the broiler chick: State of the art and outlook. Animals 11(10), 2795. https://doi.org/10.3390/ani11102795.         [ Links ]

Rodriguez de Fonseca, F., Navarro, M., Gomez, R., Escuredo, L., Nava, F., Fu, J., Murillo-Rodriguez, E., Giuffrida, A., Lo-Verme, J. & Gaetani, S., 2001. An anorexic lipid mediator regulated by feeding. Nature 414(6860), 209-212. https://doi.org/10.1038/35102582.         [ Links ]

Rudel, L.L., Parks, J.S. & Sawyer, J.K., 1995. Compared with dietary monounsaturated and saturated fat, polyunsaturated fat protects African green monkeys from coronary artery atherosclerosis. Arterioscler. Thromb. Vascul. Biol. 15(12), 2101-2110. https://doi.org/10.1161/01.atv.15.12.2101.         [ Links ]

SAS. 2012. SAS/STAT User's Guide. Statistics. SAS Institute Inc.         [ Links ]

Schepers, E., Glorieux, G., Dhondt, A., Leybaert, L. & Vanholder, R., 2009. Role of symmetric dimethylarginine in vascular damage by increasing ROS via store-operated calcium influx in monocytes. Nephrol. Dialy. Transplant. 24(5), 1429-1435. https://doi.org/10.1093/ndt/gfn670.         [ Links ]

Schulze, R., Maharaj, M., Warburton, M., Gers, C., Horan, M., Kunz, R. & Clark, D., 2007. South African atlas of climatology and agrohydrology. Water Research Commission, Pretoria, RSA, WRC Report. 1489(1), 06.         [ Links ]

Schwartz, G.J., Fu, J., Astarita, G., Li, X., Gaetani, S., Campolongo, P., Cuomo, V. & Piomelli, D., 2008. The lipid messenger OEA links dietary fat intake to satiety. Cell Metabol. 8(4), 281-288. https://doi.org/10.1016/j.cmet.2008.08.005.         [ Links ]

Speer, T., Rohrer, L., Blyszczuk, P., Shroff, R., Kuschnerus, K., Krankel, N., Kania, G., Zewinger, S., Akhmedov, A. & Shi, Y., 2013. Abnormal high-density lipoprotein induces endothelial dysfunction via activation of Toll-like receptor-2. Immunity 38(4), 754-768. https://doi.org/10.1016/j.immuni.2013.02.009.         [ Links ]

Tain, Y.L. & Hsu, C.N., 2017. Toxic dimethylarginines: asymmetric dimethylarginine (ADMA) and symmetric dimethylarginine (SDMA). Toxins 9(3), 92. https://doi.org/10.3390%2Ftoxins9030092.         [ Links ]

Tandiang, D.M., Diop, M.T., Dieng, A., Yoda, G.M.L., Cisse, N. & Nassim, M., 2014. Effect of corn substitution by sorghum grain with low tannin content on broilers production: animal performance, nutrient digestibility, and carcass characteristics. Intl. J. Poult. Sci. 13(10), 568. https://doi.org/10.1016/j.livsci.2020.104187.         [ Links ]

Thabethe, F., Hlatini, V., de Almeida, A. & Chimonyo, M., 2022. Growth performance of South African Windsnyer pigs to the dietary inclusion of amarula oil cake. Trop. Anim. Health Prod. 54(6), 343. https://doi.org/10.1007/s11250-022-03345-x.         [ Links ]

van Soest, P., Robertson, J.B. & Lewis, B.A., 1991. Methods for dietary fibre, neutral detergent fibre, and non-starch polysaccharides in relation to animal nutrition. J. Dairy Sci. 74(10), 3583-3597. https://doi.org/10.3168/jds.S0022-0302(91)78551-2.         [ Links ]

Verlengia, R., Gorjão, R., Kanunfre, C.C., Bordin, S., de Lima, T.M. & Curi, R., 2003. Effect of arachidonic acid on proliferation, cytokines production and pleiotropic genes expression in Jurkat cells - a comparison with oleic acid. Life Sci. 73(23), 2939-2951. https://doi.org/10.1016/j.lfs.2003.04.003.         [ Links ]

Yaqoob, P., Newsholme, E.A. & Calder, P.C., 1995. The effect of fatty acids on leucocyte subsets and proliferation in rat whole blood. Nutr. Res. 15(2), 279-287. https://doi.org/10.1016/0271-5317(95)92592-8.         [ Links ]

Zambón, D., Sabaté, J., Munoz, S., Campero, B., Casals, E., Merlos, M., Laguna, J. C. & Ros, E., 2000. Substituting walnuts for monounsaturated fat improves the serum lipid profile of hypercholesterolemic men and women: a randomized crossover trial. Ann. Intern. Med. 132(7), 538-546. https://doi.org/10.7326/0003-4819-132-7-200004040-00005.         [ Links ]

Zijlstra, R., Jha, R., Woodward, A., Fouhse, J. & Van Kempen, T., 2012. Starch and fibre properties affect their kinetics of digestion and thereby digestive physiology in pigs. J. Anim. Sci. 90(4), 49-58. https://doi.org/10.2527/jas.53718.         [ Links ]

 

 

Submitted 19 June 2024
Accepted 19 August 2024
Published 30 September 2024

 

 

# Corresponding author: kakade2000@gmail.com