Introduction

In animal and poultry production enterprises, feed is considered to be the most imperative and expensive element. Nowadays, the conventional energy sources used in poultry feeding have a feed-food competition and an increased demand for bio-fuel industries, which caused a continuous uprise in prices and insufficient supply. This accelerated the need to evaluate and introduce new energy alternatives for poultry to proportionally replace the expensive conventional feedstuffs.

Cassava root meal (CRM) has been reported as a promising energy alternative for poultry; mainly for its availability worldwide (Morgan and Choct 2016). It is acceptable to replace up to 50% of the poultry diets (Saree et al. 2012; Yang et al. 2010). As a crop, more than 500 million tons are produced from cassava roots yearly (FAO 2014); it represents the third largest source of carbohydrates in the world (Fauquet and Fargette 1990). Recently, the major expansion in cassava production is mainly distended to starch extraction industry, which renders large amounts of residues (Morgan and Choct 2016). During the harvesting and processing season, large amounts of CReM are rendered and most of these residues are wasted and cause environmental pollution (Gomes et al. 2005; Huyen et al. 2007; Morgan and Choct 2016).

The original CRM, the non-starch extracted, has been extensively studied as an alternative energy source in animal and poultry production. Meanwhile, there is scarce information on the potential use of cassava starch extraction residue meal (CReM), which could be utilized as an alternative energy source for poultry. The CRM was reported to contain 3000 to 3200 kcal ME/kg (Buitrago et al. 2002; Khajarern and Khajarern 2007), 5 g fiber and 70 g of starch/kg (Balagopalan 2002; Nguyen et al. 2007), 10 to 30 g/kg crude protein (Stupak et al. 2002; Chauynarong et al. 2009), and 1–2 g/kg lipids (Olugbemi et al. 2010). Additionally, resistant starches and other fermentable carbohydrates can serve as effective prebiotics for poultry, which stimulate the growth of beneficial bacteria in the gut. Some of these beneficial effects were recently reported by Poorbaghi et al. (2016).

Before offering to the animals, cassava roots are often processed by boiling, soaking, oven, or sun-drying to reduce the hydrocyanide content (HCN) (Oguntimein 1988), and the sun-drying was reported as the most effective method eradicating such cyanide (Ngiki et al. 2014). Studying the levels of plasma proteins and activity of liver enzymes of the animals fed CReM can contribute in examining the toxicity of HCN (Leeson and Summers 1988; Yang et al. 2010).

This study aims to evaluate the nutrient composition, amino acid profile, and nutritional impacts of CReM on the growth performance, carcass characteristics, internal organs, and blood metabolites of growing ducks.

Materials and methods

Birds and housing environment

In this study, a total of 960, 1-day-old, unsexed cherry valley ducklings were used. All ducklings were brooded for 10 days under the same managerial conditions. At day 11 of age, they were weighed and housed in 24 opened-floor pens, 40 ducklings each. The total area of each pen measured 27 m2, in which 18 m2 were on a slatted woody floor, plus 9 m2 as a fish pond. Feed and water were provided ad libitum, and a continuous lighting was used throughout the experiment. During the experiment period, the average cyclic temperatures ranged from 10 to 26 °C and adequate electric heaters were used properly.

Experiment design

Starting from day 11 and up to 42 days of the duck’s age, six replicate pens were assigned randomly to one of four pelleted diets; which included graded levels of CReM: (i) 0CReM (control), (ii) 50 g/kg, (iii) 100 g/kg, and (iv) 150 g/kg. The composition and chemical analyses of the tested diets and CReM are presented in Tables 1 and 2, respectively. The four diets were balanced with respect to nitrogen, energy, lysine, and methionine + cystine content (NRC 1994).

Table 1 Composition of experiment diets
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Table 2 Chemical analyses of CReM and experimental diets
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Preparation of cassava residue meal

The CReM was prepared according the method of Huyen et al. (2007). Briefly, cassava residue was collected immediately after processing the cassava root for starch production. Thereafter, it was pressed overnight to reduce the water content before being dried by the sunshine for 4 consecutive days. The final product of dried cassava residue was ground, pelleted, and stored in plastic bags until use.

Growth performance parameters

The initial and final body weights (BW) were recorded for each replicate at 11 and 42 days old, respectively. Feed intake (FI) was measured for each replicate for the whole period (between 11 and 42 days of age). Therefore, body weight gain (BWG), growth rate (GR), and feed conversion ratio (FCR) were calculated. The number of dead birds was recorded, and livability rates (%) were calculated for each treatment. The growth rate was estimated using the following formula: (total BWG) × 100/initial BW.

Carcass and internal organs

At the end of experimental period (42 days of age), 12 birds from each treatment were chosen randomly, weighed, and slaughtered. The weights of carcass, liver, gizzard, heart, spleen, ceca, and abdominal fat, as well as the lengths of ceca and small intestines, were measured. The carcass and organ weights were expressed in relation to the life BW.

Blood parameters

Two blood samples were collected, from each of the 48 slaughtered birds, in heparinized and non-heparinized tubes (10.0 mL). Total protein (TP), albumin (ALB), and triglycerides (TG) were measured in plasma samples, while alanine aminotransferase (ALT), aspartate aminotransferase (AST), and lactate dehydrogenase (LDH) were measured in the serum samples. Samples were analyzed using commercial kits purchased from Shanghai Kehua Bio-engineering Co., Ltd. (KHB) and using an autoanalyzer (SHIMADZU CL-8000 automatic autoanalyzer). Globulin (GLO) was calculated as the difference between TP and ALB. Blood metabolites were measured according to the methods of Nazifi et al. (2008).

Chemical analyses of CReM and experimental diets

The samples of CReM and experimental diets were analyzed in duplicate according to the methods of AOAC (2000).

  1. 1.

    DM was estimated by drying the CReM samples at 60 °C for 48 h in an oven with (forced air).

  2. 2.

    The nitrogen (N) content was assayed using the Kjeldahl method, which was used to calculate crude protein (CP) by multiplying N × 6.25.

  3. 3.

    Ash content was measured by igniting of the dried samples in a muffle furnace at 550 °C for 3 h.

  4. 4.

    Gross energy was analyzed using a bomb calorimeter (model HWR-15C, Shangli Instruments, Shanghai, China). The metabolizable energy nitrogen corrected (MEn) was calculated according to the following equation: MEn = 39.14 × DM − 39.14 × ash − 82.78 × CF, which was obtained from NRC (1994) (Table B–1, page 113).

  5. 5.

    The amino acid profile was estimated using the Biochrom Amino Acid Analyzer (Biochrom 30+, UK).

  6. 6.

    Calcium (Ca) was analyzed according to AOAC (2000) procedure 4.8.03.

  7. 7.

    The total phosphorus was analyzed according to AOAC (2000) procedure 3.4.11.

Statistical analysis

Data were subjected to ANOVA according to a completely randomized design (Steel and Torrie 1980), and the statistical analysis was conducted using the GLM procedure, SAS (2002). Duncan’s multiple range test (Duncan 1955) was used to compare between means wherever significant differences were found. All percentages were transformed to arcsine before analysis.

Results

Nutrient composition of CReM

The chemical analysis of CReM is shown in Table 2. The results showed that CReM contains (kg−1) 895.0 g DM, 20.0 g CP, 3306 kcal gross energy, 140.0 g CF, 60.0 g ash, 514.0 g starch, 10.6 g calcium, and 0.8 g available phosphorus. Besides, the total amino acid (AA) content (/kg) amounted to 19.9 g of CReM DM, in which the tyrosine (3.3 g), aspartic (1.9 g), glutamic (1.9 g), alanine (1.4 g), leucine (1.4 g), and proline (1.2 g) were the most occurred AAs, while the levels of methionine, cystine, isoleucine, valine, histidine, and phenyl-alanine were lower than 1.0 g/kg. In addition, the calculated MEn in the CReM was found to be 2109.54 kcal/kg.

Growth performance

The growth parameters of ducks fed graded levels of CReM are presented in Table 3. The tested CReM levels showed insignificant effects (P > 0.05) on the ducks’ growth performance and livability.

Table 3 Growth performance of ducks fed graded levels of cassava residue meal (CReM)
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Carcass and internal organs

The results of the carcass and internal organs are shown in Table 4. The dietary inclusion of CReM up to 150 g/kg did not show any adverse effect on the dressing percentage of ducks or on the relative weights of the carcass (%), internal organs (%), or abdominal fat (%). The small intestine of the control birds was relatively shorter (P > 0.05) than those fed 50 g CReM/kg and 100 g CReM/kg diet (215.75 vs. 222.58 and 226.50 cm); while it was significantly (P < 0.05) shorter than that of the 150CReM group (228.75 cm).

Table 4 Dressing percentage and internal organs of ducks fed graded levels of cassava residue meal (CReM)
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Blood parameters

The results of blood analyses are shown in Table 5. The tested CReM levels, up to 150 g/kg of the diet, did not show any significant effect on the assayed parameters in this study. However, the 50CReM and 100CReM groups tended to have higher ALT, AST, TP, and ALB levels than those of the control and 150CReM groups, but they did not reach a significance level.

Table 5 Blood analyses of growing ducks fed graded levels of cassava residue meal (CReM)
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Discussion

Nutrient composition of CReM

In the current study, the nutrient composition as well as AA profile of CReM were evaluated (Table 2). Although, the information on the CReM analysis and utilization in poultry feeding is scarce. Our results indicated that the CReM had at least 20% reduction in the starch content than the values of the original CRM, which was reported to contain 700 g of starch/kg (El-Sharkawy 2012). In addition, the obtained CF level (140.0 g/kg) in CReM was much higher than the reported range (35–50 g/kg) in the CRM (Balagopalan 2002; Lekule et al. 2007). The CP content (20 g/kg) in the CReM of the current study was in the reported range 10–30 g/kg of CRM (Stupak et al. 2002; Chauynarong et al. 2009). Moreover, our results were close to the results of Huyen et al. (2007), who found 18 g CP and 173 g CF/kg of CReM.

The CReM was found to contain a relatively higher ash (60 g/kg) than that of CRM, which estimated 41 g/kg (Ochetim 1992). The obtained calcium level in CReM was comparable to the reported CRM value of Lekule et al. (2007) as 7.0 g/kg and that of Montagnac et al. (2009) as 10.7 g/kg. The available phosphorus (0.8 g/kg) content in CReM was within the previously reported range of 0.6–1.5 g/kg in the CRM (Montagnac et al. 2009).

In the current study, the calculated MEn value in the CReM (2109.54 kcal/kg) was found to be comparable to the corresponding value of Huyen et al. (2007) as 2294.4 kcal ME/kg. On the other hand, the CReM had a lower ME content than that of CRM, which ranged between 2868 and 3200 kcal ME/kg (Muller et al. 1974; Fetuga and Oluyemi 1976; Buitrago et al. 2002; Khajarern and Khajarern 2007). This reduction in energy content obtained with CReM was expected, due to the reduced starch content (Table 2).

With respect to the AA profile, the CReM had a poor protein content in general and extremely low in some essential amino acids in particular. In this study, the total AA content in CReM was estimated to be 19.9 g/kg, which was lower than the value 25.4 g/kg reported by Nagib and Sousa (2007) with CRM. Also, the results of the current study showed that the CReM had 1.2 g lysine, 1.0 g arginine, and < 1.0 g methionine/kg. These results were in partial accordance with those of Nagib and Sousa (2007), who found the same lysine value (1.0 g/kg) and higher methionine (1.4 g/kg) and arginine levels (3.7 g/kg) than those observed in this study. The analysis of CReM in this study has confirmed the poor content of essential AAs and agreed with the reports of Muller et al. (1974), Onwueme (1978), and Olugbemi et al. (2010), which indicated that cassava roots have poor levels of methionine, lysine, tryptophan, threonine, cystine, phenylalanine, isoleucine, and proline. This shortage in the essential AA reveals the need to use supplementary AAs or a richer protein source to supplement the cassava-based diets in order to meet poultry requirements and to increase the substitution level of CReM with maize (Ngiki et al. 2014).

Growth performance

The results of the current study indicated that the dietary inclusion of CReM up to 150 g/kg had no significant effect on the duck’s growth performance (Table 3). Indeed, there is a poor literature on the utilization of CReM in poultry production versus the extensive studies on the non-starch-extracted CRM. In broilers, Huyen et al. (2007) found that the dietary inclusion of CReM up to 150 g/kg did not affect growth rate or feed conversion ratio, which goes in agreement with our results in the current study. Besides, the latter authors found that using higher CReM levels (200–250 g/kg) had adverse effects on broilers feed intake and carcass characteristics. However, based on the analysis and performance results obtained in this study with ducks, using higher incorporation levels of CReM in the diets of growing ducks seems possible. In this regard, the previous studies showed that the non-extracted CRM was acceptable at the incorporation level of 100 g/kg (Osei and Duodu 1988) and 300 g/kg (Gomez et al. 1987) in broilers, up to 600 g/kg in ducks (Saree et al. 2012; Sahoo et al. 2014), and up to 450 g/kg in geese diets (Yang et al. 2010; Sahle et al. 1992). Therefore, testing higher incorporation levels of CReM in the duck’s diets is highly recommended for evaluation. In this case, the attention should be paid to the modifications of CReM analysis versus that of CRM, including the lower energy content, the higher fiber level, and the poor amino acids. Certainly, due to the increasing interest in starch extraction of cassava roots and therefore increased availability of CReM (Morgan and Choct 2016).

The different inclusion levels of CReM in the current study had no adverse effects on the FI or FCR of growing ducks. In other studies, using high fibrous materials was reported to affect feed intake through increased dietary bulkiness and decreased energy levels. Huyen et al. (2007) reported that broilers fed high dietary levels of CReM (200–250 g/kg) consumed higher feed amount than those of lower levels (up to 150 g/kg), which was attributed to the low ME content in CReM, as birds attempt to adjust feed intake to meet their energy requirement when receiving low energy diets (Onifade and Tewe 1993). This also was concluded with laying hens fed diets included graded levels of some leaf meals (Abou-Elezz et al. 2011). The reduced DM and nutrient intake with high fibrous diets led to a reduction in the growth performance and feed conversion ratio as reported (Onifade and Tewe 1993; Jørgensen et al. 1996). However, this was not observed in the current study, where the diets were balanced to be isoenergetic and isonitrogenic. Besides, pelleting the diet had diminished the problem of increased bulkiness of the diet (Table 2).

The obtained livability and growth rate values of the birds which fed on the different CReM levels were similar to those obtained in the control group, without significant differences (Table 3). This concluded that the tested CReM was exposed to adequate processing by sun-drying, which diminished the HCN content. In other studies, an additional benefit was reported for the CM, where the use of cassava meal was reported to allow a minimal or no use of antibiotics in animal production (Kanto and Juttupornpong 2002; Tathawan et al. 2002), probably due to reduced gut colonization by Escherichia coli as suggested by Promthong et al. (2005).

Carcass and internal organs

The results of the study showed that the dietary inclusion of CReM up to 150 g/kg of ducks diet had no adverse effect on dressed weight or internal organs relative weights (Table 4). These results are in agreement with the findings of Huyen et al. (2007), who reported that using CReM up to 150 g/kg did not show any adverse effect on the broilers’ dressing percentage or carcass traits. While the same authors reported that using higher CReM levels (200 and 250 g/kg) reduced the carcass traits versus increased relative weights (%) of the digestive tract. Similarly, Sahle et al. (1992) found that including the CRM up to 450 g/kg in geese diet had no significant effect on dressed carcass percentage or carcass characteristics. Besides, the use of dietary CRM was reported to be not preferable with chicks during the early days of age. Mhone et al. (2008) reported that broilers fed diets containing 200 g cassava/kg, starting from 2 weeks of age, had higher live weight and dressed carcass than birds fed these diets from day old. Using high fibrous ingredients was reported to increase the length of the chicken’s digestive tract in several studies (Jørgensen et al. 1996; Borin et al. 2006; Abou-Elezz et al. 2012). This finding was also confirmed in the current study with CReM ducks versus those in the control group (Table 4).

Blood parameters

The measured blood parameters in the current study were mainly selected to test and imply any toxic effect related to the possible HCN residue in the CReM (Table 5). In general, the exposure to toxicants can cause an inhibition of plasma protein synthesis, mainly α and β globulins, and albumin (Espada et al. 1997). The results obtained in this study, however, indicated no significant difference in plasma TP, ALB, or GLO among the tested treatments. This implies that the tested CReM in this study was processed adequately and the HCN was reduced successfully. Yang et al. (2010) reported similar results in geese; where maize was replaced with cassava meal up to 750 g/kg of geese diet had no significant effects on serum metabolites. The liver also was reported to be affected largely by the exposure to toxicants, which increase cell membrane permeability or damage the hepatocytes, leading to elevated levels of liver enzymes secreted to the blood (Tatjana et al. 2003; Khanam et al. 2016). In another study, Khanam et al. (2016) found that the levels of liver enzymes could be increased up to 10 or 100 folds in case of liver dysfunction or hepatocyte damage. In the current study, results obtained showed some relative increase in the serum ALT and AST in the groups fed 50 g CReM/kg and 100 g CReM/kg, but it did not reach any significance level (Table 5).

To conclude, the CReM showed considerable starch and energy levels, moderate crude fiber and ash contents, and poor CP and AA contents. The dietary inclusion of CReM up to 150 g/kg had no adverse effects on the growing duck’s growth performance, dressed weight, or blood metabolites. Higher incorporation levels of CReM in the duck’s diet are recommended for future studies.