Open access peer-reviewed chapter

Activated Charcoal: A Novel Utility Product for Enhanced Animal Health and Production from Agricultural Wastes (Pig Dung and Palm Oil Wastes)

Written By

Stephen Nnaemeka Okey and Cosmas Chikezie Ogbu

Submitted: 27 May 2022 Reviewed: 30 August 2022 Published: 31 October 2022

DOI: 10.5772/intechopen.107484

From the Edited Volume

Agricultural Waste - New Insights

Edited by Fiaz Ahmad and Muhammad Sultan

Chapter metrics overview

114 Chapter Downloads

View Full Metrics

Abstract

Feed remains the most important component of the cost of production in any poultry operations. Hence, the need to harness the potentials of numerous alternative ingredients such as activated charcoal (AC) produced from agricultural wastes. The objective of the present study was to evaluate the physic-chemical properties of AC produced from a blend of agro-wastes for use as feed additives. 120 day old broilers were distributed into four treatment groups (T1-T4) of thirty birds each and were maintained on a starter and finisher diet for 3 weeks each respectively with T1 (control) fed diet containing no AC. T2-T4 was fed diet which contained 0.5, 1.0 and 1.5% of AC respectively. Physical and chemical properties of the produced AC were determined while the blood and performance parameters were determined and all data subjected to statistical analysis. The AC significantly (P > 0.05) reduced feed intake, jejunum pH, FCR, serum cholesterol levels and increased (P < 0.05) live weight gain, intestinal lengths, carcass weight and some hematological indices especially in T3 when compared with broilers fed control diet. It was concluded that AC enhanced production and health by improving on the performance, hematology of young chicks and reduction in serum cholesterol level.

Keywords

  • agricultural wastes
  • activated charcoal
  • palm fruit fibre
  • palm kernel shell
  • pig dung

1. Introduction

Feed is the most important component in any intensive poultry operation, representing about 70% of the total cost of production [1]. Hence, there is a compelling need to harness the potential of numerous alternative ingredients such as activated charcoal (AC) produced from agricultural wastes as a replacement for expensive conventional ingredients. Agricultural wastes are defined as residues from the growing and processing of raw agricultural products such as fruits, vegetables, meat, poultry, dairy products, and crops [2]. These are renewable resources whose utilization has received great attention due to environmental considerations and the increasing demand for energy worldwide [3]. Agricultural by-products are also being advocated for the production of adsorbents such as activated charcoal (AC) due to their carbon content and the possibility of mitigating environmental pollution through such a process [4]. They have also been found to be renewable and relatively less expensive when compared to other activated charcoal precursors of industrial and petroleum origin such as wood, coal, and lignite [5]. Recently, interests have focused on the use of agricultural wastes such as corn cob, groundnut shell, poultry litter, rice husk, palm kernel shell (PKS), coconut shell, and many others in the production of value-added products such activated charcoal, fertilizer, batteries, biofuel, bio-oil, and biogas [6].

The expansion of agricultural production has naturally resulted in increased quantities of livestock waste, agricultural crop residues, and agro-industrial by-products. The generation of agricultural waste will continue to increase globally as developed and developing countries continue to intensify their farming systems. Research in 2005 revealed that the biomass potential of Nigeria stood at 13 million hectares of fuel wood, 61 million tonnes per year of animal waste, and 83 million tonnes of crop residues [7]. The annual production of agricultural wastes is this high because about 94% and 68% of household are engaged in crop and livestock farming, respectively [8]. The major agricultural crops biomass feedstocks with sustainable potential in Nigeria are millet, yam, cassava, sorghum, rice, groundnut, oil palm, sugar cane, and soybeans [9]. On livestock, the estimates made in 2001 gave the total number of cattle, sheep, goats, horses, pigs, and poultry in Nigeria as 245 million, which altogether produce 0.78 million tonnes of animal waste daily as reported by Akorede et al. [8].

Oil palm industry has been recognized for its contribution toward economic growth and development in Nigeria and Malaysia. That notwithstanding, it has also contributed to environmental pollution due to the production of large quantities of waste products during the product extraction. During the processing of palm oil, more than 70% (by weight) of the processed fresh fruit bunch was left over as oil palm waste consisting majorly of extracted fiber and palm kernel shell [10]. Palm kernel Shell (PKS) are the shell fractions left over after the nut has been removed after crushing in the oil palm mill. There is a surplus of these by-products in the palm oil value chain but their utilization is extremely very negligible. Apart from a few isolated cases where they serve as a source of fuel in cooking, the PKS, for example, are usually dumped in the open field and water ponds which impact negatively on the environment [10]. Therefore, the production of activated charcoal from palm kernel shells using the process of pyrolysis could be a value addition to palm oil processing which is a veritable economic activity in Nigeria and Malaysia [11].

Pyrolysis of agricultural waste is desirable as a large part of the crop body is non-edible and goes as waste. Straw makes up to 50% of the yield of cereal crops and has more potential for char production compared to wood [12]. Different varieties of agricultural wastes that have been tested for pyrolysis include cotton cocoon, groundnut shell, nutshell, palm kernel shell, corn stalk, bagasse, banana leaves, cotton seedcake, garlic stem, pepper stem, tobacco waste, sunflower bagasse, sorghum bagasse, and cassava peels (Figure 1) [12, 13].

Figure 1.

Methods of conversion of agricultural waste to produce activated charcoal and other products using thermo-chemical and biochemical processes.

AAFCO [14] defined activated charcoal as a dark-colored porous form of carbon made from organic parts of plant or animal substances by their incomplete combustion. They are processed carbon materials that are capable of adsorbing various substances because of their highly developed pore structure and large internal specific surface area [15, 16]. It is differentiated from elemental carbon by its high surface area and the oxidation of the carbon atoms found at both its outer and inner surfaces [17]. The surface chemistry of activated charcoal confers on it the ability to absorb many gases, aqueous liquid, and poisons [16, 18, 19]. Several studies have shown that activated charcoal is harmless even when it is accidentally consumed, inhaled, or comes in contact with the skin. Although no allergic effects have been associated with its use, the American Academy of Clinical Toxicology, AACT [20] however recommended that activated charcoal should not be taken longer than 12 weeks without stopping. When mixed with water and swallowed to counteract poisoning, activated charcoal adsorbs the poison or drug, inactivating it, and then carries it inert through the entire length of the digestive tract out of the body [16, 19, 21].

Majewska [22] carried out experiment to determine the effect of hardwood charcoal supplementation on the performance and carcass characteristics of broiler at varying inclusion level in the diet. The results showed that at 3% dietary supplementation, the birds were 5% and 3.5% heavier than the control and the dressing percentages and the relative weights of the muscles were also improved at 21 and 42 days, respectively. The author attributed the results to the detoxifying effects of charcoal, thereby lowering the surface tension of the intestinal digest to support liver function with respect to fat digestion. More so, the adsorption properties of charcoal act curatively on the gastrointestinal tract (GIT), adsorbing gases such as hydrogen sulphide and ammonia that are formed there, including bacterial toxins and mycotoxins produced by fungi [23]. Jiya [24] supplemented activated charcoal at 0.5% in broiler feeds and noted increased relative organ weights and reduced cholesterol level of carcass which he attributed to efficient mineral uptake and nutrient utilization.

Durunna et al. [25] reported improved growth rates and reduced flatulence, fly population, and litter odor at varied inclusion levels of wood charcoal in the feed of broiler birds. In another research by Dim et al. [26] to ascertain the effect of dietary supplementation of activated charcoal on growth, hematology, and serum lipid profiles of broilers, the final body weight, average daily weight, and FCR favored birds placed on 6% charcoal inclusion than other groups and the control after 56 days trial period.. More so, Dim et al. [26] noted that the white blood cell (WBC) count and the packed cell volume (PCV) were not affected at both the starter and finisher phases. However, the hemoglobin concentration (Hb) and the red blood cell count were significantly improved [27, 28], while the cholesterol and lipoprotein levels were significantly reduced with no effect on triglyceride at both phases [29].

Advertisement

2. Materials and methods

2.1 Ethical approval

The Animal Ethics Committee of the College of Veterinary Medicine, Michael Okpara University of Agriculture Umudike approved to this experiment.

2.2 Location of the study

The study was carried out at the Teaching and Research Farm of Michael Okpara University of Agriculture Umudike, Umuahia, Abia State, located within the South East agro-ecological zone of Nigeria.

2.3 Study layout

The research was divided into two studies. Study 1 involved the production of activated charcoal from a blend of locally available agricultural residues such as pig dung, palm kernel shell, and palm fruit fiber and the evaluation of the physicochemical properties. Study 2 involved the evaluation of the effect of dietary inclusion of activated charcoal on growth, carcass yield, hematology, and serum biochemical indices of broiler chickens.

2.4 Collection, drying, and blending of agricultural residues

The palm kernel shell and palm fruit fiber were collected from a palm oil mill while freshly voided pig dung was collected from pig farms using a plastic container. The materials were carefully collected to avoid contamination with sand or other objects. Each material was sun-dried to constant weight and crushed manually using a wooden pestle and mortar. The materials were then blended together at a ratio of 4:3:3 weight for pig dung, palm kernel shell, and palm fruit fiber, respectively, and used to produce the activated charcoal.

2.5 Study 1 (production of activated charcoal)

The physical method of activated charcoal production described by Gunamartha and Widana [30] was employed in the present study. The blended biomass materials were weighed using HN 289 digital scale (Omron Co., Ltd., Japan) and transferred to a clay pot of about 30 liters for carbonization. In addition to contributing to the carbon yield, palm kernel shell and palm fruit fiber also served as combustion accelerants enhancing the pyrolysis of pig dung [31]. The pot containing the precursors was sealed by covering with a metallic lid that had a small vent which limited the entry of oxygen into the mixture. The pot was placed on open fire for a combustion period of 5 hours at which no more smoke was produced from the vent. At this point, water was introduced quickly to stop the carbonization of the biomass and achieve activation. Thereafter, the pot was tightly closed and allowed to cool. The charcoal product was then harvested, rinsed with cold water to remove ash and other debris, dried, and weighed. The dried activated charcoal was transferred to a wooden mortar and ground with pestle into fine powder and stored in an air tight polythene container for characterization and subsequent supplementation in broiler feeds produced according NRC [32] recommendations (Figure 2).

Figure 2.

Flow chat for producing activated charcoal.

2.6 Physicochemical characterization of the activated charcoal

The physical properties determined were bulk density, water holding capacity, specific gravity, moisture content, pH and oil adsorption capacity while the chemical properties were carbon, and mineral contents.

2.6.1 Determination of physical characteristics of activated charcoal

Activated charcoal yield was determined as the ratio of the weight of dried activated charcoal to the weight of precursor carbonized and values were expressed in percentage. The bulk density, water holding capacity, and specific gravity of the activated charcoal were determined according to the procedure described by Makinde and Sonaiya [33] and modified by Omede [34]. The moisture content of the activated charcoal was determined using oven dry method as described by the American Society for Testing and Materials [35] and the percentage moisture content was calculated as recommended by AOAC [36]. The pH of the activated charcoal was determined with the aid of a pH meter (HANNA Combo PH Meter, Model: HI 98129, USA) while oil adsorption capacity was analyzed according to ASTM F 726–99 [37]. The test was performed at 23 ± 4°C with the oil absorbency measured three times and an average value taken according to [38].

2.6.2 Determination of carbon and mineral contents

The concentration of macro minerals namely nitrogen (N2), calcium (Ca), magnesium (Mg), potassium (K), phosphorus (P), sodium (Na), and micro minerals namely manganese (Mn), zinc (Zn), copper (Cu), and iron (Fe) in the activated charcoal were measured using the Atomic Absorption Spectrophotometer method (Bulk Scientific, 205, India). The procedure was based on the principle that metallic elements in a ground form absorb light of the same wavelength which they emit when excited, with the amount of radiation absorbed being directly proportional to the concentration of the element present.

Advertisement

3. Results

The physical properties of the produced activated charcoal are presented in Table 1 while the chemical properties are presented in Table 2.

ParameterValue
Activated charcoal yield (%)71.0
Moisture (%)5.37
pH7.67
Bulk density (g/cm3)0.72
Water-holding capacity (%)77.46
Specific gravity0.73
Oil adsorption capacity (%)118.47
Surface area (cm2/g)587.00

Table 1.

Physical properties of activated charcoal produced from a blend of agricultural waste materials.

ParameterValue
Carbon content (%)79.43
Calcium (mg/kg)6185.11
Phosphorus (mg/kg)18,603.29
Sodium (mg/kg)1722.47
Potassium (mg/kg)10,275.48
Magnesium (mg/kg)3980.14
Manganese (mg/kg)721.00
Iron (mg/kg)996.35
Zinc (mg/kg)95.47
Copper (mg/kg)33.69
Arsenic (mg/kg)13.38
Nitrogen (mg/kg)3008.04

Table 2.

Chemical properties of activated charcoal produced from a blend of agricultural waste materials.

The table shows that 7.1 kg activated charcoal was obtained from a total of 10 kg precursor material representing 71.0% activated charcoal yield. Other physical properties were moisture content (5.3%), pH (7.67), bulk density (0.72), water-holding capacity (77.46%), specific gravity (0.73), oil adsorption capacity (118.47%), and surface area (587 cm2/g).

The carbon content and mineral composition of the activated charcoal produced in this study were as shown in Table 2.

Study 2: Evaluation of the effect of dietary inclusion of activated charcoal on growth, carcass yield, hematology, and serum biochemical indices of broiler chickens.

3.1 Methodology, experimental birds, and design

One hundred and twenty unsexed day old arbor acre strain of broilers were used. On arrival, they were distributed into four treatment groups (T1–T4) of 30 birds each with each group further replicated three times comprising of 10 birds each in completely randomized design. They were maintained ad-libitum on a starter and finisher diet for 3 weeks each, respectively, with T1 (control) fed diet containing no activated charcoal. T2–T4 was fed diet which contained 0.5 g/kg, 1.0 g/kg and 1.5 g/kg of activated charcoal, respectively. Data collected were feed intake, live weight, carcass weight and organ weight. Live weight gain and feed intake were used to calculate the feed conversion ratio (FCR). Blood samples were collected at the end of 1st, 4th and 6th week of the experiment from the wing vein of the birds into EDTA (Ethylene-diamine tetra-acetic acid) and plain bottles for hematological and serum biochemical analysis, respectively. The erythrocyte was counted using the hemocytometer method as describe by Schalm et al. [39] while the hemoglobin concentration was determined according to the techniques described by Cole [40]. In determining the packed cell volume (PCV), the Wintrob microheamatocrit tube method was used while other hematological indices were calculated according to the formula reported by Schalm et al. [39]. Serum biochemical tests were carried out using Randox commercial test kit specific for each biochemical parameter in accordance with standard procedures prescribed by the producer Randox Laboratories (UK). The serum parameters analyzed include the following included total serum protein, serum albumin and globulin, urea, serum creatinine concentration, alanine aminotransferase (ALT), aspartate aminotransferase (AST), alkaline phosphatase activity (ALP), total bilirubin content and total serum cholesterol. Weights of carcass and organ were determined by first slaughtering 12 birds (one per replicate) by severing of the neck with a sharp knife and removal of feathers [41]. Both the carcass and organ weights were expressed as percentage of live weight and data collected were subjected to statistical analyses using ANOVA.

Tables 3 present the growth performance of the experimental birds while Table 4 shows the relative organ weights and intestinal parameters of the broiler chicken at 1, 4, and 6 weeks of age.

AgeParametersExperimental groups
T1T2T3T4
Day 1Live w. (g)37.80 ± 2.1438.07 ± 2.4137.73 ± 2.1337.43 ± 2.46
Wk 1Live w. (g)180.00 ± 36.72197.33 ± 18.77219.33 ± 16.26194.33 ± 11.15
Weight gain120.57 ± 1.30118.63 ± 1.76122.27 ± 3.25199.97 ± 5.52
Feed intake30.33 ± 2.37b28.82 ± 2.74a29.19 ± 1.24ab28.33 ± 1.72a
FCR1.74. ±0.011.68 ± 0.071.67 ± 0.031.65 ± 0.05
Wk 4Live w (g)933.00 ± 115.881059.67 ± 148.291070.67 ± 102.811053.33 ± 153.81
Weight gain817.37 ± 20.96a886.26 ± 18.63b924.87 ± 23.10c843.27 ± 3.27a
Feed intake95.74 ± 8.12c92.70 ± 7.97bc89.28 ± 10.34ab85.93 ± 9.58a
FCR1.83 ± 0.05d1.61 ± 0.03c1.47 ± 0.03a1.53 ± 0.02b
Wk 6Live w. (g)1947.67 ± 55.08a2027.67 ± 26.41ab2114.33 ± 80.21b1988.33 ± 17.04a
Weight gain959.83 ± 54.62976.67 ± 17.891000.33 ± 44.58964.37 ± 48.34
Feed intake156.49 ± 8.00b150.92 ± 6.72a150.96 ± 5.67a153.05 ± 8.00ab
FCR2.07 ± 0.071.98 ± 0.071.94 ± 0.082.02 ± 0.11

Table 3.

Growth parameters of broiler chickens fed varying dietary levels activated charcoal.

AgeParametersExperimental groups
T1T2T3T4
Wk 1Live weight (g)180.00 ± 36.72197.33 ± 18.77219.33 ± 16.26194.33 ± 11.15
Gizzard+C (%)7.30 ± 0.606.69 ± 0.626.82 ± 0.337.14 ± 0.41
Gizzard (%)4.85 ± 0.22b4.09 ± 0.19a4.41 ± 0.13a4.40 ± 0.27a
Proventri (%)1.10 ± 0.180.99 ± 0250.96 ± 0.031.08 ± 0.07
Liver (%)3.53 ± 0.173.37 ± 0.463.42 ± 0.113.87 ± 0.42
Heart (%)0.72 ± 0.10a0.88 ± 0.12ab0.91 ± 0.08b0.84 ± 0.06ab
Intest. L. (cm)80.37 ± 3.89a112.33 ± 3.06b114.33 ± 9.29b124.00 ± 3.00b
Duodenal pH5.16 ± 0.065.30 ± 0.025.20 ± 0.175.29 ± 0.02
Jejunum pH5.16 ± 0.145.29 ± 0.015.23 ± 0.125.29 ± 0.04
Ileal pH5.27 ± 0.025.30 ± 0.035.29 ± 0.035.26 ± 0.02
Rectal pH5.31 ± 0.025.30 ± 0.035.30 ± 0.025.28 ± 0.04
Wk 4Live weight (g)933.00 ± 155.881059.67 ± 148.291070.67 ± 102.811053.33 ± 153.81
Gizzard+C (%)3.53 ± 0.22a3.59 ± 0.27a4.28 ± 0.15b4.08 ± 0.14b
Gizzard (%)2.47 ± 0.23ab2.30 ± 0.23a2.84 ± 0.04b2.68 ± 0.19ab
Proventri (%)0.49 ± 0.060.44 ± 0.030.53 ± 0.120.55 ± 0.01
Liver (%)2.52 ± 0.182.67 ± 0.332.91 ± 0.152.84 ± 0.36
Heart (%)0.49 ± 0.030.53 ± 0.060.53 ± 0.100.50 ± 0.05
Intest. L. (cm)148.00 ± 19.08a165.00 ± 6.56ab185.00 ± 23.26b176.00 ± 13.08ab
Duodenal pH6.02 ± 0.825.90 ± 0.365.93 ± 0.386.10 ± 0.26
Jejunum pH6.73 ± 0.25b6.43 ± 0.04ab6.17 ± 0.15ab5.29 ± 0.044a
Ileal pH7.50 ± 0.508.00 ± 1.007.17 ± 0.157.83 ± 1.36
Rectal pH8.10 ± 1.398.53 ± 0.906.60 ± 0.538.50 ± 1.47
Wk 6Live weight (g)1947.67 ± 55.08a2027.67 ± 26.41ab2114.33 ± 80.21b1988.33 ± 17.04a
Carcass. w (g)1359.64 ± 22.67a1473.67 ± 34.39ab1573.33 ± 104.64c1432.33 ± 22.68ab
Dressing %69.81 ± 0.96a72.67 ± 0.90b74.38 ± 2.33b72.03 ± 0.76ab
Gizzard+C (%)2.25 ± 0.122.30 ± 0.172.38 ± 0.112.20 ± 0.10
Gizzard (%)1.24 ± 0.09a1.56 ± 0.17b1.39 ± 0.15ab1.30 ± 0.06a
Proventri (%)0.36 ± 0.02a0.41 ± 0.02b0.36 ± 0.01a0.37 ± 0.02a
Liver (%)1.54 ± 0.061.67 ± 0.101.62 ± 0.111.68 ± 0.15
Heart (%)0.35 ± 0.020.38 ± 0.040.39 ± 0.020.35 ± 0.02
Intest. L. (cm)166.00 ± 17.06a188.67 ± 9.07ab207.67 ± 13.80b187.33 ± 6.51ab
Duodenal pH5.93 ± 0.476.03 ± 0.645.93 ± 0.315.87 ± 0.25
Jejunum pH6.83 ± 0.12c6.17 ± 0.21b6.17 ± 035b5.97 ± 0.25ab
Ileal pH7.60 ± 0.507.83 ± 0.557.93 ± 0.678.20 ± 0.30

Table 4.

Relative organ weight and intestinal parameters of broiler chickens fed varying dietary levels of activated charcoal.

Results are presented as mean ± standard deviation (n = 3). The results with different letter superscripts are significantly different (P < 0.05) from any paired mean across the row.

Results are presented as mean ± standard deviation (n = 3). The results with different letter superscripts are significantly different (P < 0.05) from any paired mean across the row.

Tables 57 present the hematological indices of the experimental birds at 1, 4, and 6 weeks of age, respectively.

ParametersT1T2T3T 4
RBC (× 106/mm3)3.19 ± 0.06a3.67 ± 0.11b3.43 ± 0.32a,b3.61 ± 0.17b
PVC (%)27.33 ± 0.58a31.33 ± 1.53b29.33 ± 2.08a,b31.67 ± 1.53b
HbC (g/dl)9.63 ± 0.15a10.80 ± 0.40b10.07 ± 0.83a,b10.87 ± 0.50b
WBC (× 103/mm3)36.50 ± 0.56a42.57 ± 3.19b40.83 ± 4.93a,b42.97 ± 1.44b
Platelet (× 103/mm3)158.00 ± 5.29161.00 ± 11.27150.67 ± 8.02160.67 ± 2.52
MCV(fL)92.96 ± 7.7090.24 ± 5.9992.32 ± 5.9193.07 ± 3.41
MCH (pg/cell)30.24 ± 0.5429.37 ± 0.4729.42 ± 1.2930.13 ± 0.04
MCHC (g/L)35.25 ± 0.2834.48 ± 0.4833.95 ± 1.1334.71 ± 1.04
Neutrophil (%)30.33 ± 1.5327.67 ± 2.3129.00 ± 2.6528.33 ± 0.58
Lymphocytes (%)63.00 ± 2.0064.67 ± 1.1663.67 ± 1.1665.00 ± 1.73
Monocytes (%)4.67 ± 0.585.67 ± 0.585.33 ± 1.534.67 ± 1.16
Eosinophils (%)2.00 ± 0.002.00 ± 1.002.00 ± 0.001.33 ± 0.58
Basophils (%)0.00 ± 0.000.00 ± 0.000.00 ± 0.000.00 ± 0.00

Table 5.

Hematological indices at 1 week of age for broiler chicks fed varying dietary levels of activated charcoal.

ParametersT1T 2T3T4
RBC (× 106/mm3)4.12 ± 0.30b3.48 ± 0.25a3.72 ± 0.33a,b3.37 ± 0.20a
PVC (%)35.67 ± 2.08b29.67 ± 2.52a32.00 ± 2.65a,b30.67 ± 2.31a
HbC (g/dl)15.03 ± 0.67b12.87 ± 0.83a13.40 ± 1.40a,b13.17 ± 0.38a
WBC (× 103/mm3)39.68 ± 2.1837.43 ± 4.6639.23 ± 1.3644.25 ± 5.16
Platelet (× 103/mm3)270.00 ± 54.53302.67 ± 10.60264.33 ± 53.31295.00 ± 6.00
MCV(fL)86.80 ± 5.1985.12 ± 1.8186.06 ± 0.9186.74 ± 2.29
MCH (pg/cell)36.59 ± 1.8637.18 ± 5.1535.99 ± 0.5837.32 ± 1.78
MCHC (g/L)42.17 ± 0.7043.72 ± 6.4341.83 ± 0.9043.08 ± 3.10
Neutrophil (%)61.67 ± 1.5358.33 ± 1.5361.67 ± 2.0858.00 ± 3.61
Lymphocytes (%)30.00 ± 2.00a36.00 ± 1.73b29.67 ± 2.52a33.67 ± 2.52a,b
Monocytes (%)5.00 ± 1.00a,b4.33 ± 0.58a5.67 ± 0.58b5.00 ± 0.00a,b
Eosinophils (%)3.33 ± 0.58b1.33 ± 0.58a3.00 ± 0.00b3.33 ± 1.16b
Basophils (%)0.00 ± 0.000.00 ± 0.000.00 ± 0.000.00 ± 0.00

Table 6.

Hematological indices at 4 weeks of age for broiler chickens fed varying dietary levels of activated charcoal.

ParametersT1T2T3T 4
RBC (× 106/mm3)4.01 ± 0.17b3.79 ± 0.14a,b3.86 ± 0.04a,b3.68 ± 0.07a
PVC (%)38.00 ± 1.00c36.00 ± 1.00b36.33 ± 0.58b34.33 ± 0.58a
HbC (g/dl)14.57 ± 0.06c14.03 ± 0.06b14.00 ± 0.20b13.27 ± 0.25a
WBC (× 103/mm3)39.77 ± 1.4638.50 ± 1.6838.70 ± 2.5537.57 ± 1.10
Platelet (× 103/mm3)254.33 ± 39.72a303.00 ± 6.56b281.00 ± 11.14a,b265.67 ± 5.51a,b
MCV(fL)95.39 ± 2.5095.02 ± 1.4694.21 ± 0.6893.39 ± 1.16
MCH (pg/cell)36.33 ± 1.4337.06 ± 1.3136.30 ± 0.1536.10 ± 1.37
MCHC (g/L)3.83 ± 0.093.90 ± 0.103.85 ± 0.033.86 ± 0.14
Neutrophil (%)53.33 ± 4.9353.67 ± 3.2254.67 ± 1.5355.33 ± 2.08
Lymphocytes (%)39.33 ± 4.7339.33 ± 4.0437.67 ± 2.0837.33 ± 2.31
Monocytes (%)4.67 ± 0.584.00 ± 0.004.67 ± 0.584.00 ± 0.00
Eosinophils (%)2.67 ± 0.583.00 ± 1.003.00 ± 0.003.33 ± 0.58
Basophils (%)0.00 ± 0.000.00 ± 0.000.00 ± 0.000.00 ± 0.00

Table 7.

Hematological indices at 6 weeks of age for broiler chickens fed varying dietary levels of activated charcoal.

Results in Table 57 are presented as mean ± standard deviation (n = 3). The results with different letter superscripts are significantly different (P < 0.05) from any paired mean across the row.

The serum biochemical indices of the experimental birds at week one, four and six are presented in Tables 810, respectively.

ParametersT 1T2T3T 4
Total protein (g/dl)2.45 ± 0.15a3.03 ± 0.34c2.56 ± 0.22ab2.97 ± 0.13bc
Albumin (g/dl)1.36 ± 0.04a1.52 ± 0.05b1.28 ± 0.02a1.55 ± 0.14b
Globulin (g/dl)1.09 ± 0.151.44 ± 0.271.28 ± 0.201.42 ± 0.17
AST (m/l)36.00 ± 6.0040.00 ± 2.6539.33 ± 5.1333.33 ± 2.89
ALT (m/l)23.33 ± 2.31ab27.33 ± 2.52b23.67 ± 2.31ab21.67 ± 2.52a
ALP (m/l)88.67 ± 5.51a90.00 ± 2.00ab97.67 ± 3.79bc99.00 ± 5.29c
Bilirubin (mg/l)0.45 ± 0.050.49 ± 0.050.43 ± 0.020.48 ± 0.07
Cholesterol (mg/dl)83.03 ± 2.31a105.11 ± 1.12b90.42 ± 2.66a85.28 ± 6.67a
Urea (mg/dl)9.37 ± 0.669.93 ± 2.339.44 ± 0.739.03 ± 0.42
Creatinine (mg/dl)0.88 ± 0.070.80 ± 0.080.87 ± 0.060.79 ± 0.05

Table 8.

Serum biochemical indices at 1 week of age for broiler chicks fed varying dietary levels of activated charcoal.

ParametersT1T2T3T 4
Total protein (g/dl)3.27 ± 0.243.26 ± 0.213.18 ± 0.283.14 ± 0.13
Albumin (g/dl)1.90 ± 0.062.09 ± 0.172.02 ± 0.351.90 ± 0.06
Globulin (g/dl)1.37 ± 0.271.17 ± 0.061.16 ± 0.101.23 ± 0.08
AST (m/l)36.33 ± 3.2138.67 ± 5.1338.67 ± 2.0835.33 ± 5.03
ALT (m/l)30.67 ± 1.1528.00 ± 3.0025.33 ± 2.5226.00 ± 6.25
ALP (m/l)91.07 ± 5.0091.60 ± 4.4492.80 ± 3.2293.13 ± 3.07
Bilirubin (mg/l)0.53 ± 0.060.52 ± 0.090.57 ± 0.040.46 ± 0.15
Cholesterol (mg/dl)103.37 ± 3.84c96.27 ± 0.71b,c92.03 ± 2.37a,b84.43 ± 9.04a
Urea (mg/dl)12.20 ± 1.8714.80 ± 0.5314.60 ± 2.2313.33 ± 1.59
Creatinine (mg/dl)0.79 ± 0.080.79 ± 0.090.87 ± 0.150.87 ± 0.17

Table 9.

Serum biochemical indices at 4 weeks of age for broiler chicks fed varying dietary levels of activated charcoal.

ParametersT1T2T3T4
Total protein (g/dl)3.46 ± 0.03c3.21 ± 0.03b3.12 ± 0.08a,b3.06 ± 0.07a
Albumin (g/dl)2.18 ± 0.08c1.92 ± 0.04b1.80 ± 0.01a1.80 ± 0.04a
Globulin (g/dl)1.28 ± 0.101.29 ± 0.031.32 ± 0.081.26 ± 0.03
AST (m/l)40.33 ± 0.58b36.67 ± 2.89a,b34.33 ± 2.08a40.33 ± 1.53b
ALT (m/l)29.67 ± 1.5327.33 ± 2.5227.00 ± 2.6528.67 ± 1.15
ALP (m/l)85.67 ± 4.0489.00 ± 3.6183.33 ± 3.0684.67 ± 2.52
Bilirubin (mg/l)0.56 ± 0.040.60 ± 0.030.58 ± 0.020.57 ± 0.03
Cholesterol (mg/dl)97.17 ± 0.95c90.87 ± 1.32b86.33 ± 5.05a,b81.50 ± 0.92a
Urea (mg/dl)9.50 ± 0.289.57 ± 0.999.17 ± 0.139.07 ± 0.21
Creatinine (mg/dl)0.84 ± 0.020.81 ± 0.040.83 ± 0.020.86 ± 0.06

Table 10.

Serum biochemical indices at 6 weeks of age for broiler chicks fed varying dietary levels of activated charcoal.

Results of Tables 810 are presented as mean ± standard deviation (n = 30). The results with different letter superscripts are significantly different (P < 0.05) from any paired mean across the row.

Advertisement

4. Discussion

4.1 Study 1

The observed activated charcoal yield of 71.0% is less than the 74.19% yield from palm kernel shell alone reported by Kong et al. [42]. The inclusion of pig dung and palm fruit fiber in the present study may have been responsible for the lower activated charcoal yield obtained. Pig dung and palm fruit fiber are lighter than palm kernel shell and may have lesser carbon contents. The moisture content of the activated charcoal obtained from this study (5.37%) was higher than the 3.43% and 3.50% reported by Okoroigwe et al. [11] and Lima and Marshal [4], respectively, for AC derived from palm fruit fiber, and poultry litter, respectively. It was also higher than that of Nwankwo [43] who recorded 3.50% as moisture content of AC from cow bone sourced from abattoirs. Kong et al. [42] investigated the moisture content of activated charcoal derived from PKS and reported a lower moisture content of 1.47%. The lower moisture contents of the AC reported by these researchers could be attributed to higher carbonization and activation temperatures which were over 600°C in each case as against the 300°C [44] employed in the present study. The AC exhibited a slightly alkaline pH value of 7.67 which was within the preferred range of 6.0–10.0 as reported for most agricultural residue-derived AC [45]. It has also been noted that acidic and slightly alkaline activated charcoals exhibited greater adsorption capacity and are more effective adsorbents when compared to those with very high pH values [46]. The pH result obtain from this study was however higher than the 6.1, 6.64, and 6.60 reported by Okoroigwe et al. [11], Evbuoman et al. [47] and Nwankwo [43], respectively, using agricultural residues as precursors for pyrolysis. The observed bulk density of 0.72 g/cm3 was higher than 0.49 g/cm3 reported by Evbuoman et al., [47] for PKS derived-activated charcoal. The value of the bulk density is however within the preferred range of 0.06–1.03 g/cm3 as recommended by Bryne and Nagle [48] for activated charcoal with high adsorption capacity and micro-porosity. The water-holding capacity of 77.46% reported in this experiment was higher than the value of 47.4% obtained by Kong et al. [42] for PKS derived activated charcoal. Mollinedo et al. [49] demonstrated the use of AC to improve the water-holding capacity of different soil samples and discovered that treatment of soil increased water retention capacity by 25% when compared with untreated control.

The AC produced in this study is suitable for increasing the water retention capacity of soil considering its high water-holding capacity. Enhanced soil water retention will improve plant nutrient availability and uptake; thereby improving crop yield [50, 51]. It will have additional fertilizer value because of its high concentration of important plant macro nutrients such as potassium and phosphorus [52]. The use of rice husk-activated charcoal to fertilize rice fields had been a common practice in Asian countries [52]. The urban encroachments on poultry facilities have resulted in increased complaints from local residents [53, 54], due to bad odor and nuisance flies. In addition, farmers incure huge economic losses associated with poor litter in poultry farms resulting from foot and leg problems, respiratory diseases, poor weight gain and inferior feed conversion [55]. The high water holding capacity of AC could be beneficial in minimizing problems associated with wet litter in livestock and poultry farms. Sashikala et al. [56] compared the odor abatement of poultry litter using three odor control products (activated charcoal, silica gel, and zeolite) under controlled environmental conditions and reported that activated charcoal and silica gel exhibited prominent adsorption or reduction in litter volatiles. Specific gravity (SG) otherwise called relative density is the ratio of the density of substances to the density of water [34]. This physical parameter plays a vital role in the transit of digesta through the gastrointestinal (GIT) tract of animals [57]. The value of the specific gravity obtained in this research 0.730 was lower than the 1.61 reported by Evbuoman et al. [47] but higher than the 0.64 reported by Okoroigwe et al. [11] for bamboo and palm kernel shell-derived activated charcoal, respectively. It should be recalled that particles with specific gravity of less than 1.20 were more likely to float in the gastrointestinal tract of animals thereby increasing their retention time while those greater than 1.50 sink leading to a reduced retention time [57, 58]. The specific gravity recorded in this study was far higher than the range of 0.33–0.46 reported by Omede [34] for conventional feed ingredients produced in Nigeria and hence may enhance the specific gravity of feeds when supplemented in rations.

The oil adsorption capacity (OAC) and surface area (SA) obtained in this experiment were 118.47% and 587cm2/g, respectively. The value for surface area is higher than the range of 248–253 cm2/g reported by Lima and Marshal [4] for AC derived from poultry litter material. The high surface area coupled with the slightly alkaline pH of 7.67 could be responsible for the high oil adsorption capacity of 118.42% observed. It has been reported that low pH values and high surface area tend to increase the oil adsorption capacity of ACs [46]. With these outstanding properties, the activated charcoal derived from this study could be beneficial for gastrointestinal de-contamination when used as feed additive [55, 59, 60, 61]. It has also been reported that low-cost materials such as palm kernel shell, palm fruit fiber, and animal wastes are good precursors for producing AC for use as adsorbents because of well-developed pore structure and high surface area responsible for extensive adsorption capacity [62, 63]. Therefore, the AC produced in this study could be suitable for use in water remediation in cases of oil spillage in oil producing communities [60]. Activated charcoal produced from readily available and renewable agricultural residues would be less expensive and serve as replacement for other more costly adsorbents imported for this and similar purposes, thereby transforming waste into wealth [5, 64]. Furthermore, natural water sources available to most communities in developing countries like Nigeria are rivers, and natural ponds mostly contaminated with heavy metals and effluents discharged from industries [61]. Studies by [65, 66] showed that such heavy metal contaminated water used in animal feeding have negative effects on performance. Activated charcoal such as produced in the present study could be suitable for purifying contaminated water for farm and domestic use by adsorption of metallic ions and bacterial toxins [59].

The value of the carbon content was 79.43% which is higher than the 65.4% reported by [42]. It is also higher than that of wood-derived activated charcoal (AC) (71.40%) and coconut shell-derived AC (60.07%) as reported by Widowati and Asnah [67] but lower than the 85.0, and 88.4% reported by Hidayu and Musa [68], and Okoroigwe et al. [11], respectively, using palm kernel shell and oil palm fiber as precursor materials. Lima and Marshal [4] pyrolysed poultry litter and recorded a carbon content of 29% which was far below the carbon content obtained in this study. The value obtained in the present experiment was however within the preferred range of 62.20–92.40% recommended by Domingues et al. [69] for activated charcoal with high degree of micro-porosity and adsorption capacity. More so, the carbon content value obtained in this study can be adjudged to be high when compared to the International Biochar Initiative (IBI) standard which requires 10% minimum organic carbon in activated charcoal [70]. The European Biochar Foundation also recommended that for any residue left after pyrolysis to qualify as activated charcoal, the carbon content should not be less than 10% [71]. Several studies have shown that the most important factors that affect carbon yield and carbon content of AC are density and nature of the carbonized material or precursor [72]. This could be the reason why different agricultural residues exhibit different physicochemical characteristics even with the same method of treatment or activation. Martinez et al. [73] observed that the texture, carbon yield and carbon content as well as development of pores of AC were strongly affected by the physical and chemical characteristics of the starting material or precursor.

The concentration of minerals evaluated in the present study were calcium (6185.11 mg/kg), phosphorus (18,603.29 mg/kg), sodium (1722.47 mg/kg), potassium (10,275.48 mg/kg), magnesium (3980.14 mg/kg), manganese (721.00 mg/kg), iron (996.35 mg/kg), zinc (95.47 mg/kg), copper (33.69 mg/kg), arsenic (13.38 mg/kg), and nitrogen (3008.04 mg/kg). These mineral concentrations were much higher than the values reported by Okoroigwe et al. [11] and that of Gunamartha and Widana [30] for PKS and cow dung-derived activated charcoals, respectively. These variations could be attributed to the nature of the starting material (precursor) which influences the mineral composition and concentration of the resulting activated charcoal [74, 75, 76]. More so, the properties of the AC and its elemental composition can be influenced by the method of activation, duration of activation, and carbonization temperature [77, 78]. The high concentration of potassium in the activated charcoal produced in this experiment could be attributed to the inclusion of palm fruit fiber as one of the precursors. Activated charcoal rich in potassium could serve as fertilizers to enrich soils for enhanced crop yield [79]. The heavy metals, for example, arsenic and the micro mineral (zinc) were within the allowable threshold for these elements in activated charcoals namely lead <150 mg/kg, copper <30 mg/kg, zinc <400 mg/kg, and arsenic <30 mg/kg [70].

4.2 Study 2

The feed intakes of broilers as seen in Table 3 were higher in the control when compared with the supplemented groups except in week 5 and in week 3 where that of the control did not vary significantly with group 2 probably because of its lowest inclusion rate. This trend of reduction in feed intake in the supplemented groups (T2–T4) was in agreement with the report of Kutlu et al. [80] who observed that activated charcoal reduced feed intake which was attributed to higher bulk density of activated charcoal supplemented feeds [81]. More so, the blackening of feeds by charcoal might cause reduction in palatability [81, 82] which could be responsible for the significant reduction in feed intakes for the supplemented broiler groups. The implication is that feedstuffs with high bulk density exhibit high water-holding capacity and absorb excess water in the gastrointestinal tract (GIT) capable of triggering satiety resulting to low feed intakes [34]. Satiety signal such as cholecystokinin (CCK) provides information about feed intake to the brain which thereby suppress appetite [83, 84, 85, 86]. As for the control group, there was a decreased expression of the satiety receptor (CCKR) that was responsible for the increased feed intakes [87]. These reductions in feed intake in the supplemented groups is expected in view of the fact that activated charcoal is a prebiotic which improve the nutrient status of animal by enabling more and efficient use of the nutrient present in the diet and not by stimulating appetite [88]. The non-significant variation in feed intake between broilers in group 1 and group 2 at 3 weeks of age may be attributed to the lowest inclusion of activated charcoal (0.5 kg/100 kg of feed) in diet of broilers in group T2 which may not have adversely affected feed intake. More so, the blackening of the feeds by charcoal at this lowest inclusion was also not too noticeable.

According to the results in Table 3, the live weight of broilers in the supplemented groups (T2–T4) was significantly higher than the control group (T1) at 6 weeks of age with the exception of group 4 that did not vary significantly with group 1. This non-significant variation between the live weights of broilers in groups T1 and T4 can be attributed to the highest inclusion level of activated charcoal in the diet of broilers in group 4 which was 1.5 kg/100 kg of feed which maximally reduced feed intake. The increment in the live weights and weight gains in group T2 and T3 as shown in Table 3 and the FCR that favored the supplemented groups were in agreement with the findings of Dim et al. [26] who reported that the final body weight, average daily weights and FCR favored birds placed on diet supplemented with activated charcoal than the control after 56 days trial period. The results were also in conformity with the report of Jiya et al. [24] whose results showed improved performance on inclusion of activated charcoal in broiler diets. The effect on live weights and weight gains were significantly better in group 3 with 10% charcoal inclusion than in group T2 and T4. These results were exactly similar with the findings of Durunna et al. [25] who recommended 1.0 kg/100 kg of the feed as the best inclusion level for broilers as against 0.6 kg/100 kg of feed by Dim et al. [26]. The live weights of broilers in group T4 were comparable to those in group T1 probably due to the high bulk density and the blackening of the broiler diets of G4 at 1.5 kg/100 kg inclusion that resulted to the lower feed intakes [80, 81, 82]. According to the results in Table 3, the feed conversion ratio (FCR) were better in group T3 than other groups especially at week 4 where it showed significant difference. The improvement in the feed conversion efficiency in the supplemented groups especially in group T3 could be attributed to the ability of the birds fed AC to maximally utilize the vitamin-mineral premix especially iron and B-complex vitamins in the diet probably due to the binding of AC with toxins and anti-nutritional factors in the gut [26].

More so, the higher intestinal length of the supplemented groups as seen in Table 4 could be responsible for their high performance due to increased area available for adsorption of nutrients coupled with the significant reductions in the pH of their jejunum at 4 and 6 weeks of age. The weight of the gizzard with content and gizzard were significantly higher in group T3 and T2, respectively, at 4th and 6th week in each case which resulted to their increased dressing percentages. The weight of the proventriculus and heart were significantly higher in groups T2 and T3, respectively, which together with gizzard are the major organs determining performance of birds and the economics of production [89]. Weight of internal organs expressed as percentage of live weight were significantly higher with respect to gizzard and gizzard with content in groups T3 and T4 at 4 weeks of age than group 2 while the gizzard of group T2 and T3 were significantly higher than the control at 6 weeks of age as shown in Table 4 as against the gizzard of the control group that was relatively higher at first week of age. More so, the weight of the heart expressed as percentage of live weight was significantly greater in the supplemented groups than the control group T1. These significant variations in weights are expected as the gut (gizzard) and heart are the major organs determining performance of birds and the economics of production [89]. The significant differences noticed in the weights of the heart in relation to live weight of the supplemented group can be attributed to the lowering effect of AC on serum cholesterol levels which may be responsible for the increased activity and weights of the heart. Activated charcoal interferes with the entero-hepatic circulation of bile acid and cholesterol, thereby lowering serum cholesterol in cases of hypercholesterolemia [90, 91]. In a related development, Shabani et al. [92] and Dim et al. [26] reported that plasma cholesterol levels were reduced in birds whose diets were supplemented with activated charcoal.

According to Table 4, there were no significant difference in the liver and proventricular weights relative to live weight between the broilers in the supplemented group and the control except at 6th week where the relative weights of the proventriculus to live weight was significantly higher in T2 than other groups. This was in agreement with the findings of Majewska and Zaborowski [93] that liver weights did not show any significant variations between the groups whose diets were supplemented with AC and control. There were no significant difference in the weights of the gizzard + contents relative to live weight between the groups at first and 6 weeks of age except at 4 weeks of age when groups T3 and T4 were significantly higher than group T1 and group T2. At 4 weeks of age, the relative weight of the gizzard to live weight was significantly higher in group 3 than other groups and at 6 weeks of age by group T3 and group T2. This higher relative weight of the gizzards to live weights in group T3 in the 4th and 6th week could be responsible for its higher performance since weight is an index of growth and performance.

At 1 week of age, hematological values (RBC, PCV, HbC, and WBC) were significantly higher in the supplemented treatment groups (T2 and T4) than the control (T1). These results were in conformity with the report of Dim et al. [26] who reported that AC inclusion in broiler feeds improved significantly the hematological indices such as hemoglobin concentration (Hb) and red blood cells counts (RBC). This trend was not the case at 4 and 6 weeks of age where T1 recorded RBC, PCV, and Hb that were significantly higher than T4. At 1 week of age, the broilers in the supplemented treatment groups (T2–T4) had better hematological picture than the control but with the continuous supplementation of activated charcoal till 6th week, it turned in favor of T1 followed by T3 signifying a negative correlation.

In accordance with Jindal et al. [82] and Evans et al. [81], the inclusion of AC in poultry feeds increased the bulk density and caused blackening of the feeds which caused some degree of unpalatability responsible for low feed intakes and subsequent reduction RBC counts, PCV and Hb especially in T4 with the highest inclusion level of AC as witnessed in the 4th and 6th week of age. The hematological components which consist of PCV, RBC, Hb, MCV, MCH and MCHC all fell within the normal range for broilers as reported by previous researchers with MCV, MCH and MCHC showing no significant differences between the supplemented treatment groups (T2–T4) and the control (T1) as shown in Tables 1 and 3. Iyaode et al. [94] reported normal hematological range for broilers as 25.60–32.50% for PCV, 8.93–10.45 g/dl for Hb and 3.53–3.80 x 106/μL for RBC count in broilers. Marcos et al. [95] reported broiler hematological references range to be 22–35% for PCV, 2.5–3.5 x 106 / μL for RBC, 7–13 g/dl for Hb and 12–30 × 103/μL for WBC. Hidayat et al. [96] recorded normal range for Hb in broilers as 6.65–7.4 g/dl while Salam et al. [97] and Sugiharto et al. [98] both reported range of hemoglobin concentration (Hb) in broilers to be between 5.18 and 9.30 g/dl.

The results were in agreement with the report of Dim et al. [26] noted that the hemoglobin concentration (Hb) and the red blood cell (RBC) count were significantly improved, while the cholesterol levels were significantly reduced in broilers whose diets were supplemented with activated charcoal. The authors attributed the ability of the birds fed activated charcoal to maximally utilize the vitamin-mineral premix in the diet especially iron and B-complex vitamins probably due to the binding of activated charcoal with toxins and anti-nutritional factors in the gut of bird. At 4 and 6 weeks of age, there were dose-dependent reductions in the serum cholesterol levels in the supplemented treatment groups (T2–T4) which were significantly lower when compared with T1 as shown in Tables 810. This was in agreement with the results of previous researchers that confirmed that serum cholesterol levels were reduced in birds whose diets were supplemented with activated charcoal [26, 92].

These reductions in serum cholesterol levels have elucidated the fact that activated charcoal could be useful in the treatment of hypercholesterolemia [90, 91]. This is achieved by its interference on entero-hepatic circulation by binding to cholesterol and cholesterol-containing bile acids in the gut, thus preventing them from being absorbed [99]. When bile acids are excreted, plasma cholesterol is converted to bile acids to normalize bile acids levels which eventually lowers plasma and serum cholesterol levels [90, 91]. It should be recalled that approximately 2/3 of intestinal cholesterol is derived from bile while just about 1/3 comes from diet [91, 99]. Hence the serum cholesterol is determined by the balance of its synthesis, catabolism and intestinal absorption [90]. The most common statin based therapy for hypercholesterolemia acts by inhibiting the HMG-CoA reductase enzyme to reduce cholesterol synthesis while activated charcoals are useful in reducing the intestinal absorption [90, 91]. Therefore, blocking intestinal absorption is a key point in hypercholesterolemia therapy. Activated charcoal used in this study was able to absorb excess of cholesterol in the intestine before it entered the blood circulation as corroborated by the reports of Joseph et al. [99] and Roosdiana et al. [91]. This is in agreement with the findings of Boonanuntansarn [100] that activated charcoal had a significant reduction on the blood cholesterol levels in 4-week old Nile Tilapia.

Ugbogo et al. [101] stated that although cholesterol plays central role in many biochemical processes where it helps to digest fats, strengthen cell membranes and make hormones, it is majorly known for its association with cardiovascular diseases. Hypercholesterolemia is a metabolic disease which is caused by an elevated total cholesterol level in blood circulation. This may result to its build up on arterial walls, hence narrowing the lumen and increasing risk of blood clots, heart attack and stroke often associated with disease like diabetes mellitus, hypertension and some form of thyroid, liver and kidney disease [91, 101]. About 40–70% of the world’s population suffers from hypercholesterolemia [102] and it had also been reported in cats and dogs [103]. A long-term treatment of this condition using a synthetic drug known as statin was associated with side effect including joint pains and liver damage [91]. It became imperative to explore alternative medication derived from natural products such as AC to overcome this problem.

At 1 week of age, the ALP, albumin, and total proteins were significantly higher in broiler groups whose diets were supplemented with activated charcoal (T2–T4). This was unlike at 6 weeks of age where the total protein and albumin level were significantly higher in T1 than in T2, T3 and T4 with its AST significantly higher than T3. According to Ugboho et al. [101], total protein and ALP levels present in the blood can be used to evaluate unexplained weight loss and symptoms of liver damage. The ALP, albumin and total protein were significantly higher in the supplemented treatment groups but the trend was not maintained at 6 weeks of age. The significant increase in the albumin and total protein levels in the control (T1) at 6 weeks of age when compared to the supplemented treatment groups (T2–T4) can be due to the metabolic demand from the liver resulting from the high feed intake [94]. Most of the biochemical parameters were within the patterns often found in avian species as reported by Marcos et al. [95]. The total proteins recorded in this study were in the range of 2.5–4.5 g/dl as cited by Thrall [104] while the ALT were in range of 19–50 μ/L as reported by Lumeji [105]. Globulin also was within the normal range for Gallus gallus specie (0.5–1.8 g/dl) as reported by Thrall [104].

Advertisement

5. Conclusion and recommendation

The study showed that the activated charcoal produced using these agricultural residues (pig dung, palm fruit fiber, and PKS) was of high physicochemical properties within the range of most activated charcoals produced for gastrointestinal decontamination, water treatment and environmental remediation. Its inclusion in broiler feed improved performance and carcass yield and could serve as alternative feed additive in view of the ban placed on sub-therapeutic inclusion of antibiotics for growth promotion due to antimicrobial resistance. The hematological and biochemical parameters examined were within the patterns often found in avian species signifying that activated charcoal is non-toxic and safe to be used in oral administration at best inclusion level of 1 kg/100 kg of feed. Therefore, the agricultural waste-derived activated charcoal used in this study is suitable for improvement of hematological parameters in young chicks and in cases of hypercholesterolemia to bind cholesterol and cholesterol-containing bile acids in the gut. It could also serve as a replacement for the synthetic drug used for this condition which is currently very expensive coupled with their long standing side effects which have generated a lot of complaints from patients.

Advertisement

Acknowledgments

The authors wish to express their gratitude to Prof. Charles I. Okoli of the Department of Animal Science and Technology, Federal University of Technology Owerri, Nigeria for his effort in correcting the manuscript and for providing all the technical supports.

Advertisement

Conflict of interest

The authors wish to declare that there is no conflict of interest whatsoever in this chapter contribution.

References

  1. 1. Makkar HPS, Beever P. Optimization of feed use efficiency in ruminant production systems. In: Proceedings of the FAO Symposium; 27 November 2013; Bangkok, Thailand. 2013
  2. 2. Obi FO, Ugwuishiwu BO, Nwakaire JN. Agricultural waste concept, generation, utilization and management. Nigerian Journal of Technology. 2016;35(4):957-964
  3. 3. Balat M, Kirtary E, Balat H. Main routes for the thermo-conversion of biomass into fuels and chemical. Part 1: Pyrolysis systems. Energy Conversion and Management. 2009;50:3147-3157
  4. 4. Lima IM, Marshal WE. Granular activated carbons from broiler manure: physical, chemical and adsorptive properties. Journal of Bioresource Technology. 2004;96:699-709
  5. 5. Ahmedna M, Marshal WE, Rao RM. Production of granular activated carbons from selected agricultural by-products and evaluation of their physicochemical and adsorption properties. Bioresource Technology. 2000;71:113-123
  6. 6. Sugumauan P, Susan VP, Ravichandran P, Seshadri S. Production and characterization of activated carbon from banana empty fruit bunch and Delonix regina fruit production. Journal of Sustainable Energy and Environment. 2012;3:125-132
  7. 7. Agba MM, Ushie EF, Abam I, Agba MS, Okoro J. Developing the biofuel industry for effective rural transportation. European Journal of Scientific Research. 2010;40:441-449
  8. 8. Akorode MF, Ibrahim O, Amuda SA, Otuoze AO, Olufeagba BJ. Current status and outlook of renewable energy development in Nigeria. Nigerian Journal of Technology. 2017;36(6):196-212
  9. 9. Mohammed YS, Mustafa MW, Bashir N, Mokhatar AS. Renewable energy resources for distributed power generation in Nigeria: A review of the potential. Renewable and Sustainable Energy Reviews. 2013;22:257-268
  10. 10. Zafar, S. (2018). Palm Kernel shell as biomass resource. Available from: http://www.bioenergyconsult.com/tag/combustion. pp. 12-13
  11. 11. Okoroigwe EC, Ofomatah AC, Oparaku NF, Unachukwu GO. Production and evaluation of activated carbon from palm kernel shell for economic and environmental sustainability. International Journal of Physical Science. 2013;8(19):1036-1041
  12. 12. Okoli, I.C. (2020). Agricultural residues: Abandoned wealth being recovered by tropical research. Available from: http://researchtropica.com/agricultural-residues-abandoned-wealth-being-recovered-by-tropical-research/ [Accessed June 22, 2020]
  13. 13. Dhyani V, Bhaskar T. A comprehensive review on the pyrolysis of lignocellulosic biomass. Renewable Energy. 2017;4:35
  14. 14. AAFCO. Official Publication. USA: Association of American Feed Control Officials; 2012
  15. 15. Addul A, Aberuagba F. Comparative study of the adsorption of phosphate by activated carbon from corncobs, groundnut shell and rice husk. AUJ Journal. 2005;9(1):59-63
  16. 16. Schmidt H, Hagemann N, Draper K, Kammann C. The use of biochar in animal feeding. Peer Journal. 2019;7:e7373. DOI: 10.717/peerj.7373
  17. 17. Khan AM, Ansari R. Activated carbon preparation, characterization and applications: A review article. International Journal of Chemical Technology Resource. 2009;1(4):859-864
  18. 18. Bacaoui A, Yaacoubi A, Dahbi A, Bennouna C, Phan Tan Luu R, Maldonado-Hodar FJ, et al. Optimization of conditions for the preparation of activated carbons from olive-waste cakes. Carbon. 2001;39:425-432
  19. 19. Chyka PA, Seger D, Krenzelok EP, Vale JA. Single-dose activated charcoal. Clinical Toxicology. 2005;43(2):61-87
  20. 20. American Academy of Clinical Toxicology, AACT. Position statement and practical guidelines on the use of multi-dose activated charcoal in the treatment of acute poisoning. American Academy of Clinical Toxicology. Journal of Toxicology. Clinical Toxicology. 1999;37:731-751
  21. 21. Davis. Atherosclerosis an inflammatory process. Journal of Insurance Medicine. 2005;37:72
  22. 22. Majewska T, Pudyszak K, Koziowski K. The effect of charcoal addition to diets for broiler performance and carcass parameters. Veterinary Medicine Zootechnika. 2011;55(77):30-32
  23. 23. Bhatti SA, Khan MZ, Hassan ZU, Saleemi MK, Saquib M, Khatoon A, et al. Comparative efficacy of bentolite and activated charcoal in regulating feed transfer of mycotoxins. Journal of the Science of Food and Agriculture. 2018;98(3):888-890
  24. 24. Jiya EZ, Anyanwale BA, Ijaiya AT, Ugochukwu A, Tsado D. Effect of activated coconut shell charcoal meal on growth performance and nutrient digestibility of broiler chicken. British Journal of Applied Science and Technology. 2013;3(2):268-276
  25. 25. Durunna, C.S., Abatai, U.G and Uchegbu, C. (2018). Performance evaluation of broiler chickens fed varying levels of raw African velvet tamarind, Icheku (Dialium guineense) wood charcoal as feed additive. Proceedings of 43rdAnnual Conference of the Nigerian Society for Animal Production, 18–22 March 2018; Owerri, Imo State, Nigeria. pp. 514-516
  26. 26. Dim CE, Akuru EA, Egom MA, Nnajofor NW, Ossai OK, Ukaigwe CG, et al. Effect of dietary inclusion of biochar on growth performance, haematology and serum lipid profile of broiler birds. Agro Science. 2018;17(2):8-16
  27. 27. Moyes CD, Schute PM. Principles of Animal Physiology. 2nd ed. New York, NY: Pearson International Edition; 2008
  28. 28. Sufiriyanto NI, Emmy S. Hematological profiles and performance of broiler chickens fed on commercial feed. Journal of Animal Production. 2018;20(3):183-190
  29. 29. Bawala, T. O., Akpan, U., Ogunnowo, A.O., Fusae, O. A. and Sogunle, O. M. (2007). The influence of magnesium supplementation on the hematological profile of young West Africa dwarf goats. Proceedings of the 32nd conference of the Nigerian Society for Animal Production, 76-78
  30. 30. Gunamantha IM, Widana GAB. Characterization of the potential of biochar from cow and pig manure for genecology application. Conference Series: Earth Environmental Science. 2018;131:12-55
  31. 31. Nwokolo, C. O. and Ogunyemi, S. (2008). Empirical Study on Optimizing Recovery from Oil Palm Waste in Nigeria. In: International Conference on Renewable and Alternative Energy; March 29-April 2, 2009; Owerri, Nigeria. Books of Abstracts. p. 24
  32. 32. NRC. Nutrient Requirement of Poultry. Washington, DC: National Research Council National Academic Press; 1994
  33. 33. Makinde, O. A. and Sonaiya, E. B (2007). Determination of water holding capacity, blood and rumen fluid adsorbance of some fibrous feed stuff. In: A. Giang et al., editors. Sustainability of Livestock Industry in Oil Economy. Proceedings of the 32nd Annual Conference of the Nigeria Society for Animal Production; 28: 84-87
  34. 34. Omede, A. A. (2010). The use of physical characteristics in the quality evaluation of commercial feeds and feedstuffs [MSc thesis]. Federal university of Technology, Owerri, Nigeria
  35. 35. ASTM D 280-33. Standard Test Methods for the Hydroscopic Moisture Content of Activated Carbon. West Conshohocken, PA: ASTM; 2003
  36. 36. AOAC. The Official Methods of Analysis. 13th ed. Washington, DC: Association of Official Analytical Chemists; 1990
  37. 37. ASTM F 726-99. Standard Test Methods for Oil Adsorption Capacity of Activated Carbon. West Conshohocken, PA: ASTM International; 1998
  38. 38. Hussein M, Amer AA, Sawsan II. Oil spill adsorption using carbonized pith bagasse: Trial for practical application. International Journal of Environmental Science and Technology. 2008;5:233-242
  39. 39. Schalm OW, Jain NC, Carrol EJ. Veterinary Haematology. 3rd ed. Philadelphia, PA: Lea and Febiger; 1975. pp. 197-199
  40. 40. Coles EH. Avian Clinica Pathology. Philadelphia, PA: W.B. Sanders Company; 1986
  41. 41. Scott ML, Neshein MC, Young RJ. Nutrition of Chicken. 1st ed. Ithaca, NY: Scott and Associates; 1969
  42. 42. Kong SH, Loh SK, Bachmann RJ, Choo YM, Abdu Rahim S. Production and physico-chemical characterization of biochar from palm kernel shell. Food Science and Technology Postgraduate Colloquium, AIP Conference Proceeding. 2013;1571:749-752
  43. 43. Nwankwo IH. Production and characterization of activated carbon from animal bone. American Journal of Engineering Research. 2018;7(7):335-341
  44. 44. Prakash Kumar BG, Shivakamy K, Miranda LR, Velan M. Preparation of steam activated carbon from rubber and wood sawdust (Heveabrailienis) and its adsorption kinetics. Journal of Hazardous Materials B. 2006;l36:922-929
  45. 45. Chen X, Jeyaseelam S, Graham N. Physical and chemical properties of activated carbon made from sewage sludge. Journal of Waste Management. 2002;22:755-760
  46. 46. Madu PC, Lajide, l. Physicochemical characteristics of activated charcoal derived from melon seed husk. Journal of Chemical and Pharmaceutical Research. 2013;5(5):94-98
  47. 47. Evbuomwan BO, Abutu AS, Ezeh CP. The effects of carbonization temperature on some physicochemical properties of bamboo based activated carbon by potassium hydroxide (KOH) activation. Greener Journal of Physical Science. 2013;3(5):187-191
  48. 48. Byrne CE, Nagle DC. Carbonization of wood for advanced materials applications. Carbon. 1997;35(2):259-266
  49. 49. Mollinedo J, Schumacher JE, Chintala R. Influence of feedstocks and pyrolysis on biochar’s capacity to modify soil water retention characteristics. Journal of Analytical and Applied Pyrolysis. 2015;114:100-108
  50. 50. Van Zwieten L, Kimber S, Morris S, Chan KY, Downie A, Rust J, et al. Effect of biochar from slow pyrolysis of papermill waste on agronomic performance and soil fertility. Plant and Soil. 2010;327:235-246
  51. 51. Zheng Z, Song-da Z, Ting-giang L, Feng-Liang Z, Zhen-Li H, He-ping Z, et al. Adsorption of ammonium phosphate from aqueous solution by biochar derived from phytoremediation of plants. Journal of Zhejiang University. Science. B. 2013;14(912):1152-1161
  52. 52. Steiner C. Biochar carbon sequestration: Biorefinig Carbon Cycle Program. Athens, GA: University of Georgia; 2008
  53. 53. Nwagwu C, Ede PN, Okoli IC, Chukwuka OK, Okoli CG, Moreki J. Effect of environmental factors and structural dimension of aerial pollution gas concentrations in tropical poultry pen in Nigeria. International Journal of Applied Poultry Research. 2012;1(1):15-20
  54. 54. Okoli IC, Anyaegbunam CN, Etuk EB, Uchegbu MC, Udedibie ABI. Socio-economic characteristics of poultry business entrepreneurs in Imo State, Nigeria. Journal of Agriculture and Social Research. 2004;4(2):100-111
  55. 55. Charles EB. Litter management for confined turkeys. In: Poultry Science and Technical Guide. Vol. 41. The North Carolina Agricultural Extension Service Bulletin; 2005. pp. 3-7
  56. 56. Sashikala M, Pillai GP, Xinguang R, Stuetz M. Odour abatement of poultry litter using odour control products. Chemical Engineering Transactions. 2012;30:247-257. Available from: www.acidic.it.cet
  57. 57. Bhatti SA, Firkins JT. Kinetics of hydration and functional specific gravity of fibrous feed by-products. Journal of Animal Science. 1995;73(5):1449-1458
  58. 58. Kaske M, Hatiboglu S, Engelhadt WV. The influence of density and size of particles on rumination and passage from the reticulo-rumen of sheep. British Journal of Nutrition. 1992;67:235-244
  59. 59. Lartey RB, Acquanh F, Nketia KS. Developing national capacity for manufacture of activated carbon from agricultural waste. The Ghana Engineering. 1999;3:45-50
  60. 60. Tabbakh T, Barhoun R. Cleanup oil spills by activated carbons prepared from agricultural wastes. Indian Journal of Material Sciences. 2018;16(1):1-9
  61. 61. Tumin ND, Luqman AC, Zawani Z, Suraya AR. Adsorption of copper from aqueous solution by Elaisguineensis kernel activated carbon. Journal of Engineering Science and Technology. 2008;3(2):180-189
  62. 62. Tay JH, Chen XG, Jeyaseclan S, Graham N. Comparative study of anaerobically digested and undigested sewage sludge in preparation of activated carbons. Chemosphere. 2001;44:53-57
  63. 63. Tsai WT, Lee MK, Chang YM. Fast pyrolysis of rice husk: product yields and composition. Bio-resource Technology. 2007;98:22-28
  64. 64. Malik R, Ramtake DS, Water SR. Physico-chemical and surface characterization of adsorbent prepared from groundnut shell by ZnCl2 activation and its ability to adsorb colour. Indian Journal of Chemical Technology. 2006;13:319-328
  65. 65. Etuk IF, Ogbuewu IP, Iwuji TC, Okoli IC, Aladi NO, Williams E, et al. Physiological responses of broilers to drinking water from different sources in eastern Nigeria. International Journal of Agriculture and Rural Development. 2016;19(1):2422-2426
  66. 66. Etuk IF, Ogbuewu IP, Okoli IC, Etuk EB, Iwuji TC, Obikoonu HO, et al. Quality of different water sources used in poultry and piggery farms in southeastern Nigeria. International Journal of Agriculture and Rural Development. 2014;17(2):1847-1852
  67. 67. Widowati W, Asnah A. Biochars effect on potassium fertilizer and leaching potassium dosage for two corn-planting seasons. Agrivita. 2014;36:165-171
  68. 68. Hidayu AR, Muda N. Preparation of impregnated activated carbon from palm kernel shell and coconut shell for Co2 capture. Procedia Engineering. 2016;148:106-113
  69. 69. Domingues RR, Trugilho PF, Silva CA, DeMelo ICNA, Melo LCA, Magriotis ZM, et al. Properties of biochar derived from wood and high-nutrient biomasses with the aim of agronomic and environmental benefits. PLoS One. 2017;12:e0176884
  70. 70. EBC [European Biochar Certificate]. Guideline for a Sustainable Production of Biochar. Arbaz, Switzerland; 2012 Available from: http://www.european-biochar.org/en/download
  71. 71. International Biochar Initiative. (2017). Standardized product definition and product testing guidelines for biochar that is used in soil. International Biochar Initiative, IBI-STD-1.1.
  72. 72. Verheijen F, Diafas I, Jeffery S, Bastos A, Valde MVD. Biochar Application to Soils: A Critical Scientific Review of Effects on Soil Properties and Functions. Brussels: European Commission Joint Research Centre; 2010
  73. 73. Martinez ML, Torres MM, Guzman CA, Maestri DM. Preparation and characterization of activated carbon from olive stones and walnut shells. Industrial Crop Production. 2006;23:23-28
  74. 74. Cagnon B, Py X, Guillot A, Stoecidi F, Chambar G. Contribution of hemicelluloses and lignin to the mass and the porous properties of chars and steam activated carbons from various lignocellulosic precursors. Bioresource Technology. 2009;100(1):292-298
  75. 75. Campbell QP, Bunt JR, Kasaini H, Kruger DJ. The preparation of activated carbon from South Africa coal. Journal of the Southern African Institute of Mining and Metallurgy. 2012;112:37-44
  76. 76. Abechi SE, Gimba CE, Uzairu A, Dalltu YA. Preparation and characterization of activated carbon from palm kernel shell by chemical activation. Resource Journal of Chemical Science. 2013;3(7):54-61
  77. 77. Cetinkaya S, Sakintuna B, Yuyun Y. Formation of crystal structure during activated carbon production from Turkish Elbistan lignite. Fuel and Chemical Division and Preparation. 2003;48(1):67-69
  78. 78. Hirunpraditkoon S, Tunthong N, Ruangchai A, Nuithitku K. Adsorption capacities of activated carbons prepared from bamboo by KOH activation. World Academy of Science, Engineering and Technology. 2011;78:711-715
  79. 79. Udoetok IA. Characterization of ash made from oil palm empty fruit bunches. International Journal of Environmental Sciences. 2012;3(1):518-524
  80. 80. Kutlu HR, Unsal I, Gorgulu M. Effect of providing dietary wood (Oak) charcoal to broiler chicks and laying hens. Animal Feed Science Technology. 2001;90:213-226
  81. 81. Evans AM, Loop SA, Moritz JS. Effect of poultry litter biochar diet inclusion on feed manufacture and 4–21-d broiler performance. Journal of Applied Poultry Research. 2015;24:380-386
  82. 82. Jindal N, Mahipal SK, Mahajan NK. Toxicity of aflatoxin B1 in broiler chicks and its reduction by activated charcoal. Research in Veterinary Science. 1994;56:37-40
  83. 83. Honda K. Peripheral regulation of food intake in chickens: adiposity signals, satiety signals and others. World’s Poultry Science Journal. 2021;77(2):301-312
  84. 84. Sam AH, Troke RC, Tan TM, Bewick GA. The role of the gut/brain axis in modulating food intake. Neuropharmacology. 2012;63(1):46-56
  85. 85. Tachibana T, Matsuda K, Kawamura M, Ueda H, Khan MSI, Cline MA. Feeding-suppressive mechanism of sulfated cholecystokinin (26-33) in chicks. Comparative Biochemistry and Physiology, Part A. Molecular and Integrative Physiology. 2012;161(4):372-378
  86. 86. Wood SC. The control of food intake: Behavioral versus molecular perspectives. Cell Metabolism. 2009;9(6):489-498
  87. 87. Dunn IC, Meddle ST, Wilson PW, Wardle AS, Law AS, Bishop C, et al. Decreased expression of the satiety signal receptor CCKAR is responsible for increased growth and body weight during domestication of chickens. American Journal of Physiology – Endocrinology and Metabolism. 2013;304(9):E909-E921
  88. 88. Damron WS. Introduction to animal science, 4th edition. In: Pearson International Edition, S4 carlike publishing services. Edward Brothers and Phoenix: Colcord; 2009
  89. 89. Irshad A. Effect of probiotics on broiler performance. International Journal of Poultry Science Science. 2006;5(6):593-597
  90. 90. Neuvonen PJ, Kuusisto P, Vapaatalo H, Manninen V. Activated charcoal in the treatment of hypercholerolaemia: Dose-response relationships and comparison with cholestyramine. European Journal of Chemical Pharmacology. 1989;37:225-230
  91. 91. Roosdiana A, Vidiastuti D, Herenda H. The preventive effect of activated charcoal on HDL levels and aorta histopathological profiles in hypercholesterol rat models. Journal of Physics: Conference Series. 2019;1374:012029
  92. 92. Shabani A, Dastar B, Khomeiri M, Shabanpour B, Hassani S. Response of broiler chickens to different levels of nanozeolite during experimental aflatoxicosis. Journal of Biological Sciences. 2010;10(4):362-367
  93. 93. Majewska T, Zaborowski M. Charcoal in the nutrition of broiler chickens. Medycyna Weterynaryjina. 2003;59:81-83
  94. 94. Iyaode II, Ibrahim HO, Uwade F, Shittu MW. Hematological and serum biochemistry of broilers strains (Cobbsand Arbor-acre) fed ginger. GSC Journal of Biological and Pharmaceutical Sciences. 2020;11(2):320-326
  95. 95. Marcos BC, Fabricio PR, Hugo RM, Mara RBN, Antonio VM, Cristiane FPM. Biochemical blood parameters of broilers at different ages under thermo-neutral environment. World's Poultry Science Journal. 2012 Supplement 1, Expanded Abstract – poster presentation – chicken breeder and broiler production, 143
  96. 96. Hidayat DA, Putra SS, Widiastuti E. Red Blood Profile of Broiler Chicken Fed with Tapioca Waste Fermented with Acremoniumcharticola and/or Antibiotic. UNS: National Seminar Department of Livestock; 2016
  97. 97. Salam S, Sunarti D, Isroli. Physiological responses of blood and immune organs of broiler chicken fed dietary black cumin powder during dry seasons. JITAA. 2013;38(3):185-191
  98. 98. Sugiharto I, Widiastuti and Prabowo, N.S. Effect of turmeric extract on blood parameters, feed efficiency and abdominal fat content in broilers. JITAA. 2015;36(1):21-26
  99. 99. Joseph V, Christopher AK, James VD, Ekta P, Richard FC. A retrospective review of the prehospital use of activated charcoal. The American Journal of Emergency Medicine. 2015;33(1):56-59
  100. 100. Boonanuntanasarn S, Khaomek P, Pitasong T, Hua Y. The effects of the supplementation of activated charcoal on growth, health status and fillet composition-odor of Nile Tilapia (Oreochromis niloticus) before and after harvesting. Aquaculture International. 2014;22:1417-1436
  101. 101. Ugbogo AE, Okezie E, Ijioma SN. Introducing Biochemistry Practical. Okigwe, Imo State, Nigeria: Justman Publishers International; 2017. pp. 143-202
  102. 102. Niho MN, Mutoh M, Takahashi M, Tsutsumi K, Sugimura T, Wakabayashi K. Concurrent Suppression of Hyperlipidemia and Intestinal Polyp Formation by No-1886, Increasing Lipoprotein Lipase Activity in Min Mice. Tokyo: National Cancer Centre Research Institute; 2005
  103. 103. Xenoulis PG, Steiner JMM. Lipid metabolism and hyperlipidemia in dogs. The Veterinary Journal. 2010;183:12-21
  104. 104. Thrall MA. Hematologiae Bioquimica, Clinica Veterinaria. Sao Paulo: Roca; 2007 582 p
  105. 105. Lumeji JT. Avian clinical biochemistry.In. In: Kaneko JJ, Harvey JW, Bruss ML, editors. Clinical Biochemistry of Domestic Animals. 5th ed. SanDiego, CA: Academy Press; 1997. p. 932

Written By

Stephen Nnaemeka Okey and Cosmas Chikezie Ogbu

Submitted: 27 May 2022 Reviewed: 30 August 2022 Published: 31 October 2022