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Meta-analysis of the influence of the substitution of maize with cassava on performance indices of broiler chickens

  • Ifeanyi Princewill Ogbuewu EMAIL logo and Christian Anayo Mbajiorgu
Published/Copyright: March 7, 2023
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Open Agriculture
From the journal Open Agriculture Volume 8 Issue 1

Abstract

There are growing numbers of publications on the effect of substitution of maize with cassava (Manihot esculenta Crantz) on growth indices of broiler chickens with variable results. The purpose of this meta-analysis was to explore the influence of substitution of maize with dietary cassava on growth traits (i.e., average daily feed intake [ADFI], body weight gain [BWG] and feed conversion efficiency [FCE]) of broilers. Search done in PubMed, Google scholar and Scopus databases yielded 303 studies of which 27 were suitable for the analysis. Heterogeneity was explored by subgroup and meta-regression analyses using the following moderator variables: publication year, study continent, processing methods, cassava form, substitution level, broiler strain, number of birds per groups and treatment durations. Results show that dietary cassava reduced ADFI (mean difference [MD] = −5.19 g/day; 95% confidence interval [CI]: −8.60, −1.79; I 2 = 99%) and BWG (MD = −8.49 g/day; 95% CI: −9.65, −7.33; I 2 = 98%) and increased FCE (MD = 0.29; 95% CI: 0.24, 0.35; I 2 = 99%) in broilers compared to controls. Publication year, broiler strain, treatment durations and substitution level) influenced the outcomes of the study and explained some of the sources of heterogeneity. In conclusion, our results suggested that dietary cassava inclusion at 5% (minimum) and 62% (maximum) reduced growth performance in broiler chickens. However, more effective methods for increasing the nutrient value of cassava roots for broiler chicken feeding as well as the cassava inclusion levels for optimal productivity are required.

Keywords: broiler chickens; cassava roots; maize; growth performance; meta-analysis

1 Introduction

Maize is the primary source of energy in poultry diets. However, the use of maize for livestock feed, human food and industrial raw materials has resulted in a high cost of chicken feed with a concomitant rise in the price of chicken products [1]. Thus, for the chicken industry to be sustained, there is a need for the exploitation of other energy sources as an alternative to maize [2,3,4]. One alternative energy source is cassava. The world’s annual cassava production is estimated at 263 million metric tons [5]. The tuber is the most vital part of the cassava plant and is rich in starch. Cassava starch is relatively more digestible than cereal grain starch [6]. According to Promthong et al. [7], cassava tuber starch contains 83% level of amylopectin, a branched glucan compared to 72% contained in maize. Cassava starch also contains 18–20% amylose, which is lower than the level of 28% reported for maize starch [7,8]. Cassava root has a high potential as an alternative to maize in chicken feed despite its low in crude protein (about 4%) and amino acids when compared to maize [6]. In addition, cassava is high in fibre and low in minerals and vitamins [9]. Cassava has high proportions of resistant starch, a portion of cassava starch that resists digestion in the gastrointestinal tract of chickens [10]. The major limitation to the use of cassava in chicken feed is its higher concentrations of linamarin and lotaustralin, the main substances used in the synthesis of hydrogen cyanide (HCN), which is toxic to animals [6,9]. However, several techniques have been devised for its detoxification [11,12].

Root meals, pellets and chips are the common types of cassava root products used in poultry feeding. Cassava root chips are made by first peeling, washing and slicing into thick flakes to aid drying. Pellets are formed by grinding and hardening dried chips into a cylindrical shape. The milled form of the cassava chips is the root meal. Oso et al. [13] found that diets containing high inclusion rates of cassava (200 g/kg feed) reduced live body weight and body weight gain (BWG) in broiler chickens compared to a control diet that had maize as the main energy source. Khempaka et al. [14] found a poor feed conversion efficiency (FCE) in broiler chickens when fed diets containing high inclusion levels of cassava. An earlier investigation by Brum et al. [15] revealed that cassava can substitute 68% of maize in the diet of broiler chickens without an adverse impact on growth. However, other researchers [11,16,17] found improved growth performance traits of broiler chicken fed diets that substituted maize with cassava. The use of a meta-analytic procedure to resolve variability among studies that addressed the same objective and increase statistical power has been reported in the literature [18]. Presently, there is no meta-analysis of the impact of replacement of maize with cassava on broiler chicken productivity. Thus, the aim of this investigation was to assess the influence of the substitution of maize with cassava on broiler chicken performance using meta-analytic procedures.

2 Materials and methods

2.1 Search strategy and study selection

Studies that investigated the influence of the substitution of maize with cassava on growth traits of broiler chickens were identified from a search done in PubMed, Google Scholar and Scopus databases. Selection criteria were based on the PICO framework, where the letters in PICO stand for Population (i.e., broiler chickens), Intervention (i.e., cassava diets), Control group or comparison (i.e., diets without cassava) and Outcomes (i.e., average daily feed intake [ADFI], BWG and FCE). The search was done using the following keywords: (1) cassava, (2) growth performance and (3) broiler chickens. Reference lists of identified publications were reviewed for relevant articles. The disagreement on whether to include a study or not was resolved by consensus. Trials were used for the analysis they met the following conditions; (1) the study substituted maize with cassava root in broiler chicken diets; (2) the study was reported on at least one of the outcome variables; (3) the study had a control diet with maize as the major energy source and experimental diets that substituted maize with cassava; and (4) the study reported the mean, number of birds per dietary group and a measure of variability as numerical or graphical data. Duplicated studies and review articles were excluded from the study. Studies that did not evaluate the effect of cassava roots in broiler chickens were not eligible for the meta-analysis. Trials on broiler chickens not measured on growth traits were also excluded. Two hundred and ninety-eight (298) studies were generated from database searches and 5 additional articles were identified from reviewing the reference sections of retrieved studies. Of 303 publications, 218 were discarded after screening the titles and abstracts or because they were duplicates across the three databases. After a detailed screening of the 85 full publications, 58 were further discarded. Overall, 27 articles met the requirements and were used for the analysis (Figure 1).

Figure 1 Study selection flow chart used for the meta-analysis.
Figure 1

Study selection flow chart used for the meta-analysis.

  1. Ethical approval: The conducted research is not related to either human or animal use.

2.2 Data extraction, synthesis and statistical analysis

Information on author’s name, publication year (2004–2021), study country (Australia, USA, Sudan, Nigeria, Ghana, Thailand, Brazil, Bangladesh and Zimbabwe), study continent (Oceania, Africa, North America, South America and Asia), cassava form (chip, pellet, meal and grit), cassava processing methods (drying, fermentation, palm oil fortification, enzyme and charcoal supplementation), cassava substitution levels (low: 01–49%, medium: 50–74% and high: 75–100%), broiler strains (Ross, Cobb, Anak, Hybro, Marshall and Arbor Acres) and treatment durations (1–63 days) were retrieved from each publication that was selected for the meta-analysis. Data on the number of birds included in the control and cassava groups, as well as the means of outcome variables with their standard error (SE) or standard deviation (SD) were also retrieved. For studies that reported the SE rather than the SD, the SE was converted to SD using the methods described by Adu et al. [19] and Ogbuewu et al. [20]. A database of the 27 eligible publications was built as shown in Table 1.

Table 1

Summary of studies included in the meta-analysis

Source N Country Explanatory moderator variables Outcomes
Continent PY CF PM Strain SL NBT TD
[21] 2 Australia Oceania 2015 Pellets/chips Drying Cobb 3 >50 0–21 4, 5, 6
[17] 4 Australia Oceania 2020 Pellets Drying* Ross 1, 2, 3 >50 0–35 4, 5, 6
[22] 5 USA NA 2019 Chips Drying Cobb 1, 2 <50 0–42 4, 5, 6
[23] 4 Sudan Africa 2020 Meal Drying Ross 1 <50 0–35 4, 5, 6
[24] 5 Nigeria Africa 2012 Meal Drying Marshall 1, 2, 3 <50 0–56 4, 5, 6
[25] 2 Ghana Africa 2017 Meal Drying Cobb 3 <50 0–42 4, 5, 6
[26] 5 Nigeria Africa 2019 Meal Drying Arbor Acres 1, 2, 3 <50 0–42 4, 5, 6
[27] 3 Nigeria Africa 2017 Meal Drying Anak 3 <50 0–56 4, 5, 6
[28] 5 Nigeria Africa 2018 Meal Fermentation — 1, 2, 3 <50 0–56 4, 5, 6
[29] 11 Nigeria Africa 2016 Grits Fermentation Anak 1, 2, 3 <50 0–56 4, 5, 6
[30] 5 Nigeria Africa 2019 Meal Drying Marshall 1, 2 <50 0–56 4, 5, 6
[16] 5 Nigeria Africa 2011 Meal Drying** Hybro 1, 2 <50 0–28 4, 5, 6
[31] 6 Nigeria Africa 2015 Grits Fermentation 1, 2, 3 <50 0–56 4, 5, 6
[32] 3 Nigeria Africa 2008 Meal Fermentation 1, 2 <50 0–56 4, 5, 6
[33] 5 Nigeria Africa 2014 Meal Drying Marshall 1 >50 0–28 4, 5, 6
[34] 5 Nigeria Africa 2021 Meal Drying Anak 1, 2, 3 <50 0–56 4, 5, 6
[35] 3 Thailand Asia 2016 Pellets Drying Cobb 2 <50 0–42 4, 5, 6
[36] 5 Brazil SA 2014 Meal Drying Ross 1 <50 0–21 4, 5, 6
[37] 7 Nigeria Africa 2017 Grits Fermentation Arbor Acres 1, 2, 3 <50 0–21 4, 5, 6
[38] 7 Nigeria Africa 2017 Grits Fermentation Arbor Acres 1, 2, 3 <50 0–42 4, 5, 6
[39] 6 Nigeria Africa 2006 Meal Drying** Arbor Acres 1, 2, 3 <50 0–42 4, 5, 6
[40] 9 Nigeria Africa 2017 Meal Drying* Arbor Acres 1, 2, 3 <50 0–49 4, 5, 6
[13] 6 Nigeria Africa 2013 Meal Drying+ Marshall 1 >50 0–42 4, 5, 6
[41] 4 Bangladesh Asia 2012 Meal Drying Cobb 1, 2, 3 <50 0–21 4, 6
[42] 5 Zimbabwe Africa 2004 Meal Drying Cobb 1, 2, 3 <50 0–42 4, 5, 6
[43] 4 Nigeria Africa 2004 Meal Drying++ Anak 2, 3 <50 0–63 4, 5, 6
[44] 5 Nigeria Africa 2008 Meal Drying Anak 3 <50 0–35 4, 5, 6

  1. *Plus enzyme supplementation; **fortified with palm oil; + – plus charcoal supplementation; ++ – plus fermentation; N – treatment group; ES – enzyme supplementation; NA – North America; SA – South America; CF – publication year; PY – publication year; PM – processing methods, SL – substitution level; NBT – number of broilers per treatment group; TD – treatment duration; 1 – low; 2 – medium; 3 – high; 4 – ADFI; 5 – BWG; 6 – FCE.

2.3 Statistical analysis

Open Meta-analyst for Ecology and Evolution (OpenMEE) software of Wallace et al. [45] was used to calculate the mean difference (MD) at 95% confidence interval (CI). Random-effects model was used for the meta-analysis. Negative MD values indicate that cassava diets reduced ADFI, BWG and FCE in broiler chickens, but positive MD values connote otherwise. MD was said to be significant when the upper and lower 95% CIs did not include zero or when p < 0.05 [46]. Publication bias analysis was examined using the funnel plot asymmetry and the fail-safe number (Nfs) [47]. Heterogeneity was assessed via Q-statistic and quantified using I 2-statistics [48]. I 2-statistics of <25, 25–50 and >50% were indicative of low, medium and large (high) heterogeneities, respectively. We conducted sensitivity analysis (SA) to assess the impact of studies deemed to have an unwarranted influence on the analysed outcomes [49]. This was performed when there is evidence of heterogeneity across studies utilized for the analysis. To further explore the source of heterogeneity, meta-regression analysis and group analysis were conducted to identify the contribution of moderator variables to heterogeneity [50]. Due to low statistical power, subgroup analysis was not performed in subgroups with fewer than three publications [48].

3 Results

3.1 Characteristics of included articles

The literature search performed on the three databases yielded 303 articles of which 27 met the inclusion criteria (Figure 1). The database of the included articles is shown in Tables 1 and 2, respectively. The 27 studies used for the analysis were conducted on 5 continents, with most done in Africa (78%). The earlier article was published in 2004 and the most recent study was published in 2021. The predominant broiler strains studied were Cobb (22%) followed by Arbor Acres (19%) and Anak (19%). The most common methods for processing cassava were drying and fermentation. The duration of treatment ranged from 0 to 63 days. Root meals, pellets, grits and chips were the most common forms of cassava used in the broiler chicken industry.

Table 2

Features of 27 studies included in the meta-analysis and their percentage distribution

Moderators Categories Number of studies % Distribution in the matrix
Publication year 2005–2010 6 22
2011–2015 8 30
2016–2021 13 48
Continent
Oceania 2 7
North America 1 4
Africa 21 78
South America 1 4
Asia 2 7
Processing methods
Drying 15 56
Enzyme supplementation 3 11
Fermentation 6 22
Palm fortification 2 7
Inclusion of charcoal 1 4
Substitution level
Low 20 38
Medium 17 31
High 17 31
Broiler strain
Cobb 6 22
Ross 3 11
Marshall 4 15
Arbor Acre 5 19
Anak 5 19
Hybro 1 4
Number of birds/group
<50 birds 23 85
>50 birds 4 15
Treatment duration (days)
1–21 9 25
1–24 1 3
1–28 2 6
1–35 4 12
1–42 8 24
1–49 1 3
1–56 8 24
1–63 1 3
Cassava type
Chip 3 11
Pellet 3 11
Meal 17 63
Grit 4 15

3.2 ADFI

Data on the effect of cassava on ADFI are illustrated in Table 3. Pooled result indicates that the substitution of maize with cassava in the rations of broiler chickens reduced ADFI (MD = −5.19 g/day; 95% CI: −8.60, −1.79; I 2 = 99%) when compared to the controls. Subgroup analysis of ADFI by publication year revealed that both studies published between 2004 and 2010 (MD = −3.04 g/day; p = 0.001) and between 2011 and 2015 (MD = −15.92 g/day; p = 0.015) had significantly lower ADFI when compared to the controls. However, broiler chickens from studies published between 2016 and 2021 had comparable ADFI with the controls (MD = −0.72 g/day; p = 0.303). There was a decrease in ADFI for studies performed in Africa (MD = −7.41 g/day, p < 0.001) after excluding the other four continents which had <3 studies in their subgroups. Birds from experiments that fed dried cassava had significantly reduced ADFI, whereas those from trials that fed fermented and exogenous enzyme-supplemented cassava had similar ADFI to the controls. ADFI was decreased in broiler chickens fed diets having high levels of cassava (MD = −9.13 g/day, p < 0.021). In contrast, ADFI was not affected by low and medium cassava inclusion levels. There was a significant decrease in ADFI for trials that used Marshall (MD = −30.46 g/day, p = 0.006) and Arbor Acres (MD = −6.59 g/day, p < 0.001). Cobb and Anak compared favourably with the controls in terms of ADFI. However, there was a significant increase in ADFI for trials that used Ross (MD = 2.95 g/day, p = 0.002). Broiler chickens from studies that used <50 birds per treatment group had significantly reduced ADFI (MD = −5.81 g/day, p = 0.006) when compared to the controls. Subgroup analysis of ADFI for treatment duration revealed that broiler chickens fed cassava diets for 1–42 days had significantly lower ADFI than controls (MD = −7.09 g/day, p < 0.001). However, broiler chickens fed cassava diets for 1–21, 1–35, and 1–56 days had similar ADFI values to the controls. Birds fed cassava pellets recorded significantly higher ADFI (MD = 3.64 g/day, p < 0.001) than the controls. Broiler chickens fed cassava grits had similar ADFI (MD = −0.70 g/day, p = 0.269) with the controls. Conversely, broiler chickens fed cassava chips and root meals had significantly lower ADFI than the controls (chips: MD = −3.21 g/day, p = 0.047 and root meals: MD = −8.21 g/day, p = 0.001).

Table 3

Effect of cassava on ADFI in broiler chickens

Pooled/moderators n MD 95% CI p-Value I 2 (p-value)
Pooled 26 −5.19 −8.60, −1.79 0.003 99 (<0.001)
Publication year
 2004–2010 6 −3.04 −4.90, −1.18 0.001 96 (<0.001)
 2011–2015 8 −15.95 −28.86, −3.04 0.015 99 (<0.001)
 2016–2021 12 −0.72 −2.09, 0.65 0.303 92 (<0.001)
Continent
 Africa 20 −7.41 −11.70, −3.11 <0.001 99 (<0.001)
Processing methods
 Drying 15 −6.93 −11.84, −2.02 0.006 99 (<0.001)
 Enzyme supplementation 3 −2.10 −4.97, 0.77 0.152 97 (<0.001)
 Fermentation 6 0.79 −3.01, 4.59 0.682 92 (<0.001)
Substitution level
 Low 20 −1.40 −3.02, 0.23 0.093 95 (<0.001)
 Medium 17 −5.33 −13.53, 2.87 0.203 99 (<0.001)
 High 17 −9.13 −16.87, −1.40 0.021 99 (<0.001)
Broiler strains
 Cobb 6 0.67 −2.10, 3.44 0.634 96 (<0.001)
 Ross 3 2.95 1.12, 4.78 0.002 93 (<0.001)
 Marshall 4 −30.46 −52.13, −8.79 0.006 99 (<0.001)
 Arbor Acre 5 −6.59 −8.25, −4.94 <0.001 94 (<0.001)
 Anak 5 −0.39 −4.03, 3.25 0.834 95 (<0.001)
NBT
 <50 birds 23 −5.81 −9.97, −1.66 0.006 99 (<0.001)
 >50 birds 4 −2.05 −5.42, 1.32 0.233 98 (<0.001)
Treatment durations (days)
 1–21 9 −2.76 −5.57, 0.05 0.054 98 (<0.001)
 1–35 4 −1.66 −6.11, 2.79 0.465 97 (<0.001)
 1–42 8 −7.09 −10.33, −3.84 <0.001 94 (<0.001)
 1–56 8 −9.04 −29.01, 10.93 0.375 99 (<0.001)
Cassava form
 Chip 3 −3.21 −6.37, −0.04 0.047 94 (<0.001)
 Pellet 3 3.64 1.80, 5.48 <0.001 87 (<0.001)
 Meal 17 −8.21 −13.11, −3.32 0.001 99 (<0.001)
 Grit 4 −0.70 −3.53, 2.14 0.269 91 (<0.001)

n – Number of study; ADFI – average daily feed intake; NBT – number of chicken per treatment group; MD – mean difference; CI – confidence interval; I 2 – inconsistency index; p – probability.

3.3 BWG

Pooled estimation and subgroup analyses of the impact of dietary cassava on BWG of broiler chickens are presented in Table 4. Pooled effect size demonstrates that broiler chickens fed cassava as a replacement for maize had lower BWG (MD = −8.49 g/day; 95% CI: −9.65, −7.33; I 2 = 98%) than controls. Similarly, restricted subgroup analysis showed that publication year had significant and negative effect on BWG. Broiler chickens from studies done in Africa had significantly decreased BWG (MD = −9.46 g/day, p < 0.001) after excluding the other four study continents (i.e., South America, North America, Asia and Oceania) that had <3 studies in their strata. Processing methods, substitution level and broiler strains had a significant negative impact on BWG in broiler chickens. In addition, broiler chickens from experiments that used <50 birds and >50 birds in each treatment group had lower BWG than controls. Birds from trials that included more or less than 50 birds in each treatment group had similar BWG (<50 birds: 95% CI: −9.79, −7.33 and >50 birds: 95% CI: −10.71, −6.64). Broiler chickens from trials that fed cassava for 1–21, 1–35, 142 and 1–56 days had significantly lower BWG than controls after excluding trials that fed cassava for 1–24, 1–28, 1–49 and 1–63 days which had <3 studies in their subgroups. Broiler chickens offered cassava chips (MD = −6.82 g/day, p < 0.001), pellets (MD = −5.26 g/day, p < 0.001), grits (MD = −8.99 g/day, p < 0.001) and root meals (MD = −9.11 g/day, p < 0.001) had significantly lower BWG than the controls.

Table 4

Effect of cassava on BWG in broiler chickens

Moderators n MD 95% CI p-Value I 2 (p-value)
Pooled 25 −8.49 −9.65, −7.33 <0.001 98 (<0.001)
Publication year
 2004–2010 6 −8.37 −10.54, −6.20 <0.001 98 (<0.001)
 2011–2015 7 −14.15 −16.89, −11.42 <0.001 99 (<0.001)
 2016–2021 13 −5.87 −7.25, −4.483 <0.001 97 (<0.001)
Continent
 Africa 22 −9.46 −10.83, −8.08 <0.001 99 (<0.001)
Processing methods
 Drying 14 −8.95 −10.56, −7.34 <0.001 98 (<0.001)
 Enzyme supplementation 3 −8.28 −10.77, −5.79 <0.001 96 (<0.001)
 Fermentation 6 −7.85 −9.43, −6.26 <0.001 95 (<0.001)
Substitution level
 Low 19 −6.41 −8.07, −4.75 <0.001 98 (<0.001)
 Medium 16 −7.80 −9.81, −5.79 <0.001 97 (<0.001)
 High 16 −11.07 −13.14, −8.99 <0.001 98 (<0.001)
Broiler strains
 Cobb 5 −9.81 −12.83, −6.79 <0.001 98 (<0.001)
 Ross 3 −3.99 −5.46, −2.53 <0.001 95 (<0.001)
 Marshall 4 −19.08 −23.55, −14.61 <0.001 99 (<0.001)
 Arbor Acre 5 −8.09 −10.38, −5.80 <0.001 98 (<0.001)
 Anak 5 −6.26 −8.38, −4.14 <0.001 97 (<0.001)
NBT
 <50 birds 22 −8.46 −9.79, −7.13 <0.001 99 (<0.001)
 >50 birds 4 −8.68 −10.71, −6.64 <0.001 98 (<0.001)
Treatment durations (days)
 1–21 8 −8.52 −10.94, −6.11 <0.001 99 (<0.001)
 1–35 4 −5.07 −7.56, −2.59 <0.001 97 (<0.001)
 1–42 9 −9.95 −12.82, −7.08 <0.001 98 (<0.001)
 1–56 8 −9.32 −11.77, −6.86 <0.001 98 (<0.001)
Cassava form
 Chip 3 −6.82 −9.75, −3.89 <0.001 97 (<0.001)
 Pellet 3 −5.26 −6.84, −3.68 <0.001 91 (<0.001)
 Meal 16 −9.11 −10.80, −7.43 <0.001 99 (<0.001)
 Grit 4 −8.99 −10.65, −7.34 <0.001 95 (<0.001)

n – Number of study; BWG – body weight gain; NBT – number of chicken per treatment group; MD – mean difference; CI – confidence interval; I 2 – inconsistency index; p – probability.

3.4 FCE

The influence of cassava on FCE of broiler chickens is shown in Table 5. The mean effect estimate revealed that cassava diets increased FCE (MD = 0.29; 95% CI: 0.24, 0.35; I 2 = 99%) in broiler chickens compared to the controls. Subgroup analysis shows that publication year had significant positive effect on FCE. Broiler chickens from experiments performed in Africa had significantly increased FCE (MD = 0.31 g/g, p < 0.001) after excluding studies performed in South America, North America, Asia and Oceania which had less than three trials in their subgroups. Drying (MD = 0.20, p < 0.001) and exogenous enzyme supplementation (MD = 0.15, p < 0.001) as a processing method resulted to poor FCE, while fermentation improved FCE (MD = −2.67, p < 0.001) compared to the controls. Substitution level and treatment durations had significant positive influence on FCE in broiler chickens. There was an increase in FCE for experiments that used Cobb (MD = 0.09, p < 0.001), Ross (MD = 0.20 g/g, p < 0.001), Marshall (MD = 0.07 g/g, p < 0.001) and Arbor Acres (MD = 0.31, p < 0.001). In comparison with the controls, Anak fed cassava diets had improved FCE (MD = −2.01, p < 0.001). Broiler chickens from studies that used less or more than 50 birds per treatment group had poor FCE (<50 birds: MD = 0.29, p < 0.001 and >50 birds: MD = 0.30, p < 0.001). Similarly, broiler chickens offered cassava chips (MD = 0.21 g/g, p < 0.001), pellets (MD = 0.25 g/g, p < 0.001), root meals (MD = 0.18 g/g, p < 0.001) and grits (MD = 0.80 g/g, p < 0.001) had inferior FCE when compared to the controls.

Table 5

Effect of cassava on FCE in broiler chickens

Moderators n MD 95% CI p-Value I 2 (p-value)
Pooled 26 0.29 0.24, 0.35 <0.001 99 (<0.001)
Publication year
 2004–2010 6 0.20 0.11, 0.30 <0.001 99 (<0.001)
 2011–2015 8 0.45 0.31, 0.60 <0.001 98 (<0.001)
 2016–2021 13 0.30 0.23, 0.36 <0.001 97 (<0.001)
Continent
 Africa 20 0.31 0.24, 0.37 <0.001 99 (<0.001)
Processing methods
 Drying 15 0.20 0.15, 0.24 <0.001 99 (<0.001)
 Enzyme supplementation 3 0.15 0.08, 0.22 <0.001 94 (<0.001)
 Fermentation 6 −2.67 −3.28, −2.06 <0.001 99 (<0.001)
Substitution level
 Low 20 0.26 0.20, 0.33 <0.001 98 (<0.001)
 Medium 17 0.20 0.06, 0.34 <0.001 99 (<0.001)
 High 17 0.30 0.19, 0.40 <0.001 99 (<0.001)
Broiler strains
 Cobb 6 0.09 0.05, 0.14 <0.001 99 (<0.001)
 Ross 3 0.20 0.13, 0.26 <0.001 97 (<0.001)
 Marshall 4 0.07 −0.14, 0.28 <0.001 99 (<0.001)
 Arbor Acre 5 0.31 0.15, 0.47 <0.001 99 (<0.001)
 Anak 5 −2.01 −2.46, −1.56 <0.001 99 (<0.001)
NBT
 <50 birds 23 0.29 0.23, 0.35 <0.001 99 (<0.001)
 >50 birds 4 0.30 0.23, 0.38 <0.001 98 (<0.001)
Treatment durations (days)
 1–21 9 0.11 0.02, 0.19 <0.001 98 (<0.001)
 1–35 4 0.95 0.72, 1.17 <0.001 99 (<0.001)
 1–42 8 0.30 0.24, 0.36 <0.001 99 (<0.001)
 1–56 8 0.62 0.38, 0.86 <0.001 98 (<0.001)
Cassava form
 Chip 3 0.21 0.14, 0.28 <0.001 91 (<0.001)
 Pellet 3 0.25 0.18, 0.32 <0.001 97 (<0.001)
 Meal 17 0.18 0.11, 0.25 <0.001 99 (<0.001)
 Grit 4 0.80 0.61, 0.99 <0.001 99 (<0.001)

n – Number of study; FCE – feed conversion efficiency; NBT – number of chicken per treatment group; MD – mean difference; CI – confidence interval; I 2 – inconsistency index; p – probability.

3.5 Meta-regression analysis and funnel plot asymmetry

Tables 3–5 show evidence of large heterogeneity (I 2-index = 98–99%) across studies used for the analysis. In addition, there is minimal proof of funnel plot asymmetry (Figures 2–4). The relationship between moderators and outcome measures is shown in Table 6. Publication year (Q M = 14.1, R 2 = 8, p = 0.029) and broiler strains (Q M = 44.8, R 2 = 23, p < 0.001) were linearly related to ADFI. There was significant linear relationship between aspects of studied moderators (i.e., publication year, broiler strains and substitution level) and BWG in broiler chickens. Publication year (Q M = 7.06, R 2 = 3, p = 0.029) and treatment durations (Q M = 131, R 2 = 46, p < 0.001) were predictors of the effect cassava treatment on FCE in broiler chickens.

Figure 2 Funnel plots of the impact of cassava intervention on ADFI in broiler chickens.
Figure 2

Funnel plots of the impact of cassava intervention on ADFI in broiler chickens.

Figure 3 Funnel plots of the impact of cassava intervention on BWG in broiler chickens.
Figure 3

Funnel plots of the impact of cassava intervention on BWG in broiler chickens.

Figure 4 Funnel plots of the impact of cassava intervention on FCE in broiler chickens.
Figure 4

Funnel plots of the impact of cassava intervention on FCE in broiler chickens.

Table 6

Relationship between measured outcomes and moderator variables in broiler chickens fed cassava

Outcome Moderator variables Estimate Q M DF p-Value R 2
ADFI Publication year −16.02 14.1 2 0.001 8
Continent 1.80 6.34 4 0.175 2
Processing methods −6.94 3.75 4 0.441 0
Substitution level −9.16 3.97 2 0.137 1
Broiler strains 0.77 44.8 5 1.56 × 10−8 23
NBT −2.02 0.66 1 0.418 0
Treatment durations −2.86 3.48 8 0.901 0
Cassava form −3.00 6.27 3 0.099 2
BWG Publication year −14.198 8.36 2 <0.001 10
Continent −6.97 8.73 4 0.068 3
Processing methods −8.97 1.47 4 0.831 0
Substitution level −11.09 6.76 2 0.034 3
Broiler strains −9.83 35.2 5 1.37 × 10−6 19
NBT −8.65 0.01 1 0.940 0
Treatment durations −8.62 5.82 7 0.558 0
Cassava form −6.80 2.61 3 0.455 0
FCE Publication year 0.50 7.06 2 0.029 3
Continent 0.29 0.58 4 0.965 0
Processing methods 0.21 8.84 4 0.065 3
Substitution level −1.36 1.49 2 0.475 0
Broiler strains 0.11 7.42 5 0.192 2
NBT 0.30 0.47 1 0.494 0
Treatment durations 0.11 131 7 0.000 46
Cassava form 0.21 2.17 3 0.538 0

R 2 – Proportion of heterogeneity explained by the variable; DF – degree of freedom; Q M – coefficient of moderators; NBT – number of chicken per treatment group; FCE – feed conversion efficiency; BWG – body weight gain; ADFI – average daily feed intake; p – probability.

4 Discussion

The results of this meta-analysis revealed that the substitution of maize with cassava in broiler chicken diets reduced growth indices. The mechanism by which cassava could impair growth in broiler chickens is not well established. However, it could be that the residual HCN contained in cassava diets binds cytochrome c oxidase, a respiratory energy-transducing enzyme in the mitochondria, resulting in tissue hypoxia. It is also possible that the high fibre content of cassava root-based diets contributed in part to the poor performance of broiler chickens fed cassava diets. High-fibrous diets have been demonstrated to increase feed bulkiness, reduced feed intake, and as a result, lead to depress weight gain in broiler chickens [43,51]. The poor FCE in broiler chickens fed cassava diets compared to controls in the present study supports the findings of Bokanga [52], who reported that residual HCN in cassava diets reduces the efficiency of feed digestion and nutrient utilization by lowering the lengths of the small intestine [53]. The significant decline in the growth of broiler chickens on cassava diets supports the findings of Aladi [11], who observed depressed weight gain in broiler chickens fed fermented cassava diets.

The fact that most of the trials used in the present analysis were conducted between 2016 and 2021 suggests that the use of cassava in the chicken diet is on the rise. This could be attributed to the rising price of major energy feed resources, especially in developing countries, which encourages the search for close alternatives, such as cassava [54]. Meta-analysis results showed a small effect for publication year as a moderator and explained 21% of between-study variability on the target variables. Our results indicate that broiler strain influenced the outcomes of the study and explained 23% and 19% of between-study variability for ADFI and BWG, respectively. Our results tended to show that Ross, Cobb, Anak, Marshall and Arbor Acres fed cassava diets had impaired growth performance, presumably due to the poor nutritional quality and digestibility of cassava diets. Therefore, more research is needed to identify broiler strains with the potential to utilize cassava diets, particularly in Africa where the majority of the trials used for the meta-analysis were performed.

The significantly higher ADFI in broiler chickens offered cassava pellets in this study agrees with Bhuiyan and Iji [21], who found that broiler chickens fed cassava pellets had better growth indices than those offered cassava chips. Cassava is high in resistant starch and crude fibre, which limit digestion and nutrient utilization in chickens [55]. Cassava chips and root meals are less processed than cassava pellets and may contain a higher level of HCN and non-digestible fibre. Our results show that broiler birds fed cassava grits had comparable ADFI with the controls, implying that cassava grit had similar nutrient content to maize. The impaired BWG and FCE in broiler chickens offered cassava pellets, chips, grits and root meals when compared to the controls in the present investigation could be related to the poor capability of cassava to increase nutrient digestibility and uptake in the chicken gut, leading to a reduction in muscle protein accretion. This agrees with the results of Khempaka et al. [14], who noticed poor FCE in birds fed increasing levels of cassava diets.

The extent to which animals utilize the nutrients contained in cassava is determined by processing techniques and animal factors [55]. In this meta-analysis, the inability of drying, exogenous enzyme supplementation and fermentation as a processing method to improve chicken performance suggest that these methods were ineffective in reducing the cyanide levels in cassava tuber to a safe level [56]. The observed results also tend to reaffirm the findings of others [11,43], who demonstrated that sundried or sundried fermented cassava cannot substitute maize in broiler chicken diets without negatively impacting performance. Conversely, Bhuiyan and Iji [21] reported improved BWG in broiler chickens fed cassava diets supplemented with enzyme admixture. Likewise, Chang’a et al. [17] observed enhanced growth in broiler chickens fed cassava rations supplemented with multi-enzyme. One possible explanation is that these single trials appear to lack sufficient sample size and consequently statistical power to detect the true effect of cassava intervention on growth traits of broiler chickens. Low statistical power reduces the likelihood of detecting a true treatment effect and results in a false-negative trial result—a type II statistical error [57]. Thus, more innovative techniques are advocated to enhance the feeding value of cassava in broiler chickens.

The current meta-analysis found significant effect of substitution level and treatment durations on BWG and FCE, respectively. Our results also revealed that broiler chickens given diets containing low, medium and high substitution levels of cassava for 1–21, 1–35, 1–42 and 1–56 days had impaired growth performance. This could be linked to the adverse effect of residual HCN present in the cassava diets on nitrogen retention and amino acid absorption in the jejunum and ileum. Cassava is also high in non-digestible fibre and resistant starch [55], which could limit nutrient digestibility and utilization in the small intestine of chicken. In this study, the negative influence of cassava-based diets on growth characteristics was observed both in studies with more or less than 50 broiler chickens. In contrast, there was no significant linear relationship between moderators (continent, cassava form, processing methods and number of birds per dietary group) and growth traits in broiler chicken fed cassava diets. This means that continent, cassava form, processing methods and number of birds per dietary group were not good predictors of the impact of cassava on growth traits in broiler chickens.

Large heterogeneity was found across trials that explored the effect of cassava on our outcomes of interest, which SA and subgroup analyses could not resolve. Meta-regression analyses suggest that covariates accounted aspects of heterogeneity in the present study. Publication bias exists when the outcome of a trial influences the decision of the journal editor or reviewers to publish or not [58]. The MDs plotted against the SE found gaps in the funnel plots for ADFI and BWG. The Nfs shows the number of unpublished non-significant articles that would be needed to change the significantly pooled results to non-significance [59]. Jennions et al. [60] stated that the outcomes of meta-analysis can be deemed robust in spite of publication bias when the Nfs is >5 (n = number trials used for the analysis) + 10. In the present study, the Nfs for the database was 158 times greater than the thresholds required to consider the pooled results robust. In light of this, publication bias is of no consequence in the current study as a huge number of unpublished or un-retrieved non-significant or null results articles to change the statistically significant effect of cassava intervention on ADFI and BWG in broiler chickens to non-significance.

5 Conclusion

Our results suggest that dietary cassava inclusion at 5% (minimum) and 62% (maximum) in the diets broiler chicken diets reduced growth performance traits. Cassava inclusion in the diet was only affected by its substitution level, publication year, broiler strain and treatment durations for growth variables. Considering the escalating cost of maize, there is a need to devise more effective methods for improving the feeding value of cassava roots in broiler chickens. However, the best substitution levels of cassava that support optimal performance in broiler chickens need to be determined using the quadratic optimization model.

  1. Funding information: The authors state no funding involved.

  2. Author contributions: The authors conceived, designed the methodology and prepared the manuscript. Data extraction, analysis, visualization and manuscript draft were performed the authors. All authors read and approved the final manuscript.

  3. Conflict of interest: The authors state no conflict of interest.

  4. Data availability statement: All data generated or analyzed during this study are included in this published article.

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Received: 2022-08-20
Revised: 2022-12-24
Accepted: 2022-12-28
Published Online: 2023-03-07

© 2023 the author(s), published by De Gruyter

This work is licensed under the Creative Commons Attribution 4.0 International License.

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https://doi.org/10.1515/opag-2022-0166
Keywords for this article
broiler chickens; cassava roots; maize; growth performance; meta-analysis
Creative Commons
BY 4.0

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