Efficacy of mycosorbents to ameliorate the adverse effects of natural aflatoxin contamination in the diets of Cherry Valley ducks

K Rattanasinthuphong, B Tengjaroenkul, U Tengjaroenkul and P Pakdee

Khon Kaen University, Khon Kaen 40002, Thailand
btengjar@kku.ac.th   ;   parpak@kku.ac.th

Abstract

This study was conducted to determine efficacy of mycosorbents to ameliorate adverse effects of natural aflatoxins contaminating diets of Cherry Valley ducks. A total of 144, seven-day-old ducks were randomly allotted into 4 treatments: (1) basal diet; (2) aflatoxins-contaminated diet (AFD); (3) AFD + 0.2% hydrated sodium calcium alumino silicate (HSCAS); and (4) AFD + 0.2% multi-mycosorbents (Thai bentonite, clinoptiolite and yeast cell wall) (MM). There were 3 replications of 12 birds in each treatment. Feed and water were provided ad libitum throughout the 42 day study period. At the end of the study, body weights were measured for the calculation of productive performance, and blood samples from 6 ducks per treatment were collected to determine hematological and serum biochemical parameters.

Ducks fed AFD had lower productive performance, hematological and serum biochemical parameter values (P<0.05). Supplementation of 0.2% HSCAS and 0.2% MM to the AFD improved productive performance, hematology and serum biochemistry parameters (P<0.05), as compared with the AFD (P<0.05). These results indicated that 0.2% HSCAS and 0.2% MM alleviated the toxic effects of AF in Cherry Valley ducks; however, 0.2% MM showed better improvement than 0.2% HSCAS.

Keywords: adsorbent, binder, growth, mycotoxin, poultry, serum

Introduction

Mycotoxins are toxic secondary metabolite produced by fungi that can cause illnesses and economic losses to livestock animals (Zain 2011). Maize is the main source of energy in poultry diets in Thailand. However, producers have some limitation to its use because maize can be easily contaminated with molds. Currently, there are at least two mycotoxins contaminating animal feed ingredients, and their synergistic interactions can enhance the deleterious effects on growth performance, hematology, biochemistry and immunity (Gowda et al 2008, Schatzmayr and Streit 2013). Aflatoxin (AF) is a major problem in poultry production, and ducks are highly susceptible to AF more than chickens (Bintvihok 2001). The most potent dietary approach to preventing the negative effects of aflatoxins (AFs) in poultry is to use mycosorbents (Surai and Dvorska 2005). Various sorbent products are available on the commercial markets, such as single ingredients of clay, bentonite, zeolite, hydrated sodium calcium alumino silicates (HSCAS), or combinations of sorbent materials either enzyme or yeast-derived or both (Kossolova et al 2009, Zhao et al 2010, Neef et al 2013,Tengjaroenkul et al 2013). However, there is no clear evidence that the efficacy of these products and their functions is well understood. Therefore, the purpose of this study was to determine the efficacy of two types of mycosorbents (HSCAS and MM) to ameliorate the adverse effects of natural aflatoxins on growth performance, hematology, and serum biochemistry in Cherry Valley ducks.

Materials and Methods

Animals, experimental design and management

A total of 144, seven-day-old mixed-sex (6:6 ratio of male to female) Cherry Valley ducks were purchased from a commercial hatchery (Charoen Pokphand Foods, Public Company Limited, Thailand). The ducks were weighed to calculate an average initial bodyweight, and they were randomly allocated to each of 4 treatments with 3 replications each, using a completely randomized design (CRD). Treatments were as followings: (1) basal diet, control group (fed maize-soybean meal); (2) aflatoxins contaminated diet (AFD); (3) AFD + 0.2% hydrated sodium calcium alumino silicate (HSCAS) as a reference toxin binder (ALCA Co., LTD. Bangkok, Thailand); and (4) AFD + 0.2% multi-mycosorbents (MM)(mixture of Thai bentonite, clinoptiolite and yeast cell wall). The ducks were managed under an open house system at a poultry research station, Department of Animal Science, Khon Kean University, and were provided feed and water ad libitum. Overhead lighting was set up as 12 hours daily throughout the 42 day experiment, and all experiments were conducted in accordance with the principle and guidelines approved by the Institutional Animal Care and Use Committees of Khon Kaen University.

Analysis of mycotoxins

Concentrations of AFB₁ and AFB₂ contamination in maize and diets were determined by High Performance Liquid Chromatography (HPLC)(in-house method based on Association of Official Analytical Chemists (AOAC, 2005). Other mycotoxins (deoxylevalinol (DON), fumonisin (FUM), ochratoxin (OTA), zearalenone (ZEN)) were not included in this study because they either had very low levels or were undetected.

Feed ingredients

Ingredients and feed formulations of starter phase (d 1-d 21) and grower phase (d 22- d 42) in duck diets are presented in Table 1. The calculated nutrient compositions are based on Nutrient Requirements of Poultry: Ninth Revised Edition (NRC, 1994) recommendations for duck diets. The proximate analyses of the experimental diets were performed according to the procedures of AOAC (1990).

Productive performance determination

The ducks’ health was examined, and mortality rate was recorded. Ducks were weighed at 42 days of age, and feed intake was recorded for calculation of body weight gain (BWG), average daily weight gain (ADG), average daily feed intake (ADFI), feed consumption ratio (FCR), coefficient of variation of body weight (CVBW), survival rate
(SVR), and European production efficiency factor (EPEF).

Hematological and serum biochemical analyses

At the end of the study, 4 mL of blood samples from 3 birds per replication of each treatment were taken from the wing vein for analysis of blood hematology, i.e. pack cell volume (PCV) and hemoglobin (Hb) concentration, and serum biochemistry, i.e. glucose, cholesterol, total protein, alanine aminotransferase (ALT), aspartate aminotransferase (AST), alkaline phosphatase (ALP), lactate dehydrogenase (LDH), calcium (Ca) and phosphorus (P) using Roche/Hitachi cobas c501 automatic analyzer.

Organ weights

At the end of the experiment, 3 birds per replication of each treatment were humanely euthanized. Weights of liver, kidney, heart and gizzard were recorded, then they were adjusted to 100 g of live body weight (g/ 100 g of BW), and the mean values were calculated.

Statistical analyses

All data were analyzed using the GLM procedure of ANOVA in the SAS software (SAS Institute, 1998) for completely randomized designs. The differences in means were compared using Duncan’s Multiple Range Test (DMRT) and statements of statistical significance were based on P<0.05.

Results

Mycotoxin concentrations

In the present study, the contaminated maize contained AFB₁ and AFB₂ levels at 62.42 µg/kg and 18.11 µg/kg, respectively. Upon preparation for experimental diets, the aflatoxins contaminated diets (AFD) at the starter phase contained 32.22 µg/kg AFB₁ and 11.29 µg/kg AFB_2, and AFD at the grower phase contained 38.12 µg/kg AFB ₁ and 13.16 µg/kg AFB₂. These AF levels were higher than that recommended by the US Food and Drug Administration (FDA) and the European Union (EU), which specified a maximum level of AFB₁ content of 20 µg/kg in poultry diets (Kamalzadeh et al 2009, Yang et al 2014).

Productive performance

Productive performance indicators are summarized in Table 2. At 42 d, the ducks fed AFD (treatment 2) had lower BWG, ADG, ADFI, FCR, SVR, EPEF and CVBW (P<0.05) when compared with the control and other treatments. Supplementation with 0.2% HSCAS and 0.2% MM in AFD increased BWG, ADG, ADFI, SVR, EPEF (P<0.05), and improved FCR, CVBW of the ducks (P<0.05). However, the FCR in 0.2% MM supplementation group was better than that of 0.2% HSCAS treatment (P<0.05).

Hematology and serum biochemistry

Hematological and serum biochemical parameters are presented in Table 3. At 42 d, hematological parameters of the ducks fed AFD had lower PCV and Hb values (P<0.05) when compared with the other treatments. Supplementation with 0.2% HSCAS and 0.2% MM in AFD increased PCV and Hb concentration (P<0.05) when compared with the AFD. However, both mycosorbents could not completely ameliorate the toxic effects of AFD on PCV and Hb to the same level as in the control treatment.

For serum biochemistry, the ducks fed AFD had lower glucose, cholesterol, total protein, Ca and P levels (P<0.05), and increased levels of ALT, AST, ALP and LDH (P<0.05) when compared with the control and other treatments. Supplementation with 0.2% HSCAS and 0.2% MM in AFD had increased the levels of glucose, cholesterol, total protein, Ca and P (P<0.05), and decreased levels of ALT, AST, ALP and LDH (P<0.05) when compared with the AFD.

Organ weights

Organ weights are presented in Table 4. Weights of liver, kidney and heart in the AFD treatment increased (P<0.05), but weight of the gizzard was decreased (P<0.05) as compared with the control. Supplementation with 0.2% HSCA and 0.2% MM in the AFD did reduce weights of liver, kidney and heart (P<0.05), and increased weight of the gizzard (P<0.05). However, only 0.2% MM supplementation in AFD completely ameliorated the toxic effects of AFD by enhancing the weights of all organs similarly to those in the control treatment.

Discussion

Productive performance

This study demonstrated that mycotoxins contaminated diets had adverse effects on productive performance and decreased BWG, ADG, ADFI, EPEF, SVR, while increasing FCR and CVBW in Cherry Valley ducks (P<0.05). Similar findings were observed by Han et al (2008), who reported that AFB ₁ (20 and 40 μg/kg) in contaminated diets decreased BWG, ADFI, and increased FCR, and also altered activities of duodenal gut enzymes in ducks (P<0.05). Li et al (2012) reported that feeding AFB₁ (98.73 μg/kg) decreased BW and ADG (P<0.05) in the Cherry Valley ducks. He et al (2013a) reported that the Cherry Valley ducks fed diets contained AFB₁ (196.8 μg/kg) linearly and quadratically decreased ADG, ADFI (P<0.05), and linearly and quadratically increased mortality rate as the toxin concentrations increased (P<0.05). According to Wan et al (2013), animals receiving natural maize contaminated with AFB₁ (170 μg/kg) had linearly decreases in ADG and SVR, and increased CVBW (P<0.05) as dietary AFB₁ increased. Chen et al (2014) demonstrated that Pekin ducks fed AFB₁ (110, 140, and 210 μg/kg) had decreased FI and BWG (P<0.05). Khajarern et al (2003) reported that ducks fed AFB₁ (120 μg/kg) diets had decreased FI, BWG, SVR (P<0.05), and lower FCR (P<0.05), but ducks fed AFB₁ (30 to 60 μg/kg) had no negative effects on FI, BWG and FCR (P>0.05). Cheng et al (2001) reported that Mule ducklings fed AFB₁ 200 μg/kg diet had decreased ADFI, ADG (P<0.05), and increased FCR (P<0.05). Chang et al (2016) reported that AFB₁ (80-81 μg/kg) in the diet had decreased BW, ADG and FI (P<0.05), and increased FCR (P<0.05), plus reduced development of the breast and thigh muscles in Cherry Valley ducks.

Hematology and serum biochemistry

Blood hematology and serum biochemistry parameters can be used to evaluate health status, liver function and nutritional deficiencies of animals (Quist et al 2000). In this study, AFD created advert effects by decreasing the level of PCV and Hb values (P<0.05), when compared with the control diet. Similarly, Khajarern et al (2003) found that contaminated diets containing AFB₁ (30-120 μg/kg) decreased PCV (P<0.05), and that diets of AFB₁ (60-120 μg/kg) decreased Hb level in the Cherry Valley ducks (P<0.05). Li et al (2012) reported that Cherry Valley ducks fed AFB₁ (98.73-103.61 μg/kg) contaminated diet had decreased Hb, mean corpuscular Hb levels and platelets (P<0.05). He et al (2013a) reported that the AFB₁ contaminated diets decreased Hb, PCV and red blood cell counts (P<0.05) in ducks as AFB₁ concentrations increased. The reduction of PCV and Hb indicating an anemic condition was observed probably because of AFs toxicities causing the necrosis or altering hemopoietic processes (formation of blood cellular components by stem cell) in the bone marrow (Birbrair and Frenette 2016). Jenkins and Smith (2003) reported that anemia could occurred due to an increase in the rate of erythrocyte destruction in the hematopoietic organs, or the dysfunction of enzyme activities involved in heme biosynthesis (erythropoiesis, hemosynthesis and osmoregulatory processes)(ATSDR 2005).

In this study, AFD alone caused increased levels of AST, ALT, ALP and LDH activity, and decreased levels of Ca and P (P<0.05) in serum of the Cherry Valley ducks as compared with the control diet. These findings agreed with Bintvihok and Davitiyananda (2002) who reported that Cherry Valley ducks fed AF contaminated diets had higher levels of the enzymes ALT, AST and LDH (P<0.05). Han et al (2008) reported that AFB ₁ (20-40 μg/kg) increased activities of ALT and AST (P<0.05) in the Cherry Valley ducks, while Chen et al (2014) found that AFB ₁ (110-210 μg/kg) was associated with a linearly increased of ALP and AST (P<0.05) in Pekin ducks, as AFB₁ level increased. Li et al (2012) reported that feeding AFB₁ (98.73 μg/kg) contaminated diet increased ALP (P<0.05), but decreased levels of ALT and AST (P<0.05) in Cherry Valley ducks. He et al (2013a, 2013b) reported that ducks fed AFB₁ (130.5-157.1 µg/kg) in diets increased serum LDH (P<0.05). Méndez-Albores et al (2007) reported that ducks fed 100 ppb AFB₁ had increased AST and ALT activity as well as the AST:ALT ratio (P<0.05). Cheng et al (2001) reported that Mule ducklings fed AFB₁ (200 μg/kg) contaminated diets had increased levels of AST and ALT (P<0.05), but the level of ALP was not affected (P>0.05). Shi et al (2015) reported that AFB₁ induced oxidative damage, cellular morphological changes, mitochondrial swelling, and mitochondrial DNA damage of liver cells of ducklings. This was consistent with the results of Liao et al (2015) who reported that AFB ₁ induced dysfunction and apoptosis in liver cells, and also increased levels of serum ALT and AST in ducklings (P<0.05). Bintvihok and Davitiyananda (2002) reported that ducks fed AF contaminated diets had higher levels of serum enzyme ALT, AST and LDH (P<0.05). In this study, the AFD treatment had negative effects by increasing levels of AST, ALT, ALP and LDH activity. This occurred probably because the AFB₁ residues in the liver induced oxidative stress in cells by generating free radicals (Reactive Oxygen Species) causing cell and DNA damage, impairment of protein function, and eventually leading to many chronic diseases as well as cancer (Hayes and McLellan 1999, Kotan et al 2011).

In this study, AFD alone caused lower the levels of serum Ca and P in Cherry Valley ducks (P<0.05) and similar findings were observed by Chen et al (2014), who found that feeding AFB₁ (110-210 μg/kg) contaminated diets was associated with a linearly decrease in Ca and P levels (P<0.05) in Pekin ducks, as AFB₁ increased in diets. Khajarern et al (2003) reported that ducks fed AFB₁ (60 and 120 μg/kg) contaminated diets had decreased levels of Ca and P (P<0.05), but ducks fed AFB₁< 30 μg/kg contaminated diet were not affected by lower levels of Ca and P (P<0.05). Han et al (2008) also reported that AFB₁ (20-40 μg/kg) contaminated diets had no adverse effect on the levels of Ca and P in ducks (P > 0.05), as compared with the control diet.

Additionally, this study showed that AFD had adverse effects by decreasing the levels of the total serum protein, cholesterol and glucose concentration in Cherry Valley ducks (P<0.05) when compared with the control diet. Similar findings were observed by Chen et al (2014) who found that feeding AFB₁ (110-210 μg/kg) contaminated diets linearly and quadratically decreased serum total protein and glucose concentrations in Pekin ducks (P<0.05), as AFB₁ concentrations increased. He et al (2013a) found that AFB₁ diets linearly decreased serum cholesterol and triglyceride of ducks (P<0.05), while Li et al (2012) reported that AFB₁ contaminated diets decreased levels of total cholesterol, triglycerides and blood urea nitrogen in ducklings (P<0.05) when compared with the control group. Wan et al (2013) reported that AFB ₁ contaminated in duck diets linearly decreased serum albumin (P<0.05), and linearly and quadratically decreased levels of total protein and globulin (P<0.05), and also decreased villus height and villus-crypt ratio in small intestine of the ducks (P<0.05). Han et al (2008) found that AFB₁ (20-40 μg/kg) contaminated diets decreased digestibility of crude protein (P<0.05), and increased activities of enzymes, protease, chymotrypsin, trypsin and amylase in the duodenum content of ducks (P<0.05), but the increase of these enzymes was abnormal and pathologic, and did not enhance nutrient digestibility in the ducks. In the present study, AFD decreased the levels of total protein, cholesterol and glucose, which may be a consequence of reduction of FI in the AFD treatment, or it could be that AFB₁ restrained protein synthesis (Jindal et al 1994, Rosa et al 2001, Kubena et al 2004, Zhao et al 2010). AFD treatment may interfere with the formation of enzymes necessary for metabolism of energy, protein and fat (Osweiler 1996) or may be impairment of hepatic lipogenesis, hepatic function and its metabolism or may change hepatic gene expression, biotransformation and the immune system gene (Yarru et al 2009, He et al 2013a).

Organ weights

Liver and kidney are the major target organs for the detoxification and metabolism of AFs in poultry (Del Bianchi et al 2005). According to previous studies by Miazzo et al (2005), Bailey et al (2006), and Pasha et al (2007), the liver is where most AFs are bio-activated to the reactive 8, 9-epoxide form, which could bind DNA, RNA and proteins in liver organ, then damaged the liver cells and increased the liver weight.

The present study found that the AFD group increased weights of liver, kidney, heart and gizzard (P<0.05), when compared to control group. These results are similar to several studies including Khajarern and Khajarern (2003), who reported that AFB₁ (60 to 120 μg/kg) increased organ weights in Cherry Valley ducks. He et al (2013b) reported that ducks fed AFB₁ contaminated diets (130.52-157.13 μg/kg of AFB₁) had increased liver and spleen weights (P<0.05). The increase of internal organ weights (liver, heart, kidney, spleen and pancreas) in poultry was due to congestion of blood during the inflammatory response, and probably because of tissue hypertrophy after exposed to the mycotoxins (Bondy and Pestka 2000, Khajarern and Khajarern 2003, Oswald et al 2005). However, several previous studies found that increases in natural AFB₁ in the diets of ducklings (during 1-3 wk) linearly decreased organ weights of the liver, spleen, thymus and bursa of Fabricius (P<0.05). Wan et al (2013) reported that chronic exposure to AFB ₁ negatively affected growth performance and organ development leading to a reduction of liver weight in ducklings.

Mycosorbent

In present study, supplementation with 0.2% HSCAS or 0.2% MM ameliorated the adverse effects of AFB₁ on productive performance, hematology and serum biochemistry parameters in Cherry Valley ducks (P<0.05). These results agreed with previous studies reporting that HSCAS, a phyllosilicate clay of the smectite class can reduce the bioavailability of AFs as well as prevent AFs absorption through the gastrointestinal (GI) tract by binding β-carbonyl portion of the AF molecule to the uncoordinated edge site of aluminum ions in HSCAS. This make the AF molecules pass harmlessly through the animal (Phillips et al 1990, Araba and Wyatt 1991, Ramos and Hermandez 1997, Ledoux et al 1999). Previous studies by Li et al (2012), reported that the addition of 0.1% calcium montmorillonite to AFB₁ (98-104 μg/kg) diets in ducks showed improvement of hematology, serum biochemistry and antioxidant status of ducklings when compare to AFD. Wan et al (2013) reported that 0.1% modified calcium montmorillonite supplementation in AFB₁ (30-99 μg/kg) improved productive performance, serum protein and immunoglobulin, relative organ weight, intestinal morphology and mortality in ducklings (P<0.05). Yang et al (2014) found that 0.1% calcium montmorillonite in contaminated diets (52-104 μg/kg of AFB₁) reduced the toxic effects of AFB₁ by improved apparent digestibility and true digestibility of glycine and protein in the ducks (P<0.05).

Rosa et al (2001) reported that broilers fed 5 mg/kg AFB₁ mixed with 0.3% sodium bentonite showed a higher ability to binding AFB ₁ in vitro, and also improved BWG, FCR, biochemical parameter and relative organ weights (kidney and spleen)(P<0.05). Miazzo et al (2005) reported that supplementation 0.3% sodium bentonite to AFB ₁ (2.5 ppm) and fumonisin B₁ (200 ppm) in broiler diets could reduce the deleterious effects of toxic diets, particularly, weight gain, organ weight, serum biochemistry and liver. Bintvihok et al (2002, 2003) reported that supplementation of esterified glucomannan (EGM) from the yeast cell wall (YCW) of Saccharomyces cerevisiae in AFB ₁ contaminated diet could reduce the liver injury including bile proliferation and fatty degeneration in ducklings. Gowda et al (2008) reported that supplementation 0.5% HSCAS to the AFB₁ (1 mg/kg of AFB₁) diet improved AVFI, BWG, liver weight (P<0.05) and liver antioxidant status, and also reduced the severity of hepatic lesions in broilers. Similarly, Neeff et al (2013) found that supplementation 0.5% HSCAS to the AFB₁ (2.5 mg/kg) decreased the bioavailability of AFB₁ by reduction of toxin residues in liver and kidney in broilers. Chen et al (2014) reported that 0.5% HSCAS supplementation in AFB₁ (0.5-2 mg/kg) feed could reduce the negative effects of AFB ₁ in broilers by improving BWG, liver weight, serum biochemistry and antioxidant functions (P<0.05).

However in present study, we found that 0.2% MM improved the FCR and EPEF better than 0.2% HSCAS. This occurred probably due to the fact that MM contained a combination of three ingredients of different types of mycosorbents including: (1) bentonite clay, an inorganic montmorillonite having high ability to adsorb AFs molecule (Grenier and Applegate 2013); (2) clinoptiolite, a natural inorganic zeolite that can adsorb to AFs, OTA) and ZEN (Grenier and Applegate 2013, Wu et al (2013); and (3) yeast cell wall (YCW) or mannans and glucans polysaccharides that can bind to AFs, OTA and ZEN by hydrogen and van der Waals bonds as well as ionic or hydrophobic interactions at the β-1,3 glucan backbone with β-1,6 glucan side chains (Yiannikouris et al 2003, 2004, Shetty et al 2007, Guan et al 2011, Grenier and Applegate, 2013). Furthermore, YCW can also stimulate immunization, serum biochemistry, and increase the population of intestinal microflora in animals. Huwig et al (2001) reported that use of single mycosorbent products could not be effective again most types of natural mycotoxins, but apply a combination of different mycosorbents would provide a more versatile tool for preventing mycotoxicosis. Azizpour and Moghadam (2015) reported that YCW-derived glucomannan prepared from Saccharomyces cerevisiae was shown to efficiently binding AFs, FUM and ZEN. Girish and Devegowda (2006) reported that supplementation of 0.1% glucomannan from YCW ameliorated the toxic effects of the individual and combined toxicity of AFB₁ and trichothecene toxin (T-2) by enhancing growth performance, organ weight and antibody titer (P< 0.05), while 1% HSCAS was only beneficial to AFB₁. Similarly, Che et al (2011) reported that 0.05% esterified glucomannan from YCW and 0.2% HSCAS, supplementation in AFB₁ diet could alleviate hematological and serum biochemical parameters, liver antioxidant status and liver morphology of broilers.

Conclusions

• AFB₁ (32.22-38.12 μg/kg) contaminated diets cause negative effects on growth performance, hematology and serum biochemistry parameters in Cherry Valley ducks.
  
  
•  Supplementation with 0.2% HSCAS or 0.2% MM ameliorated the adverse effects of the toxins; however, 0.2% MM demonstrated better preventive results than 0.2% HSCAS.

Acknowledgements

The authors gratefully acknowledge the Division of Research and Technology Transfer Group, Khon Kaen University, and the Research Group in Toxic Substances in Livestock and Aquatic Animals, Faculty of Veterinary Medicine, Khon Kaen University for the financial support. We thank Dr. Frank F. Mallory, Laurentian University, Canada for reviewing the manuscript.

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Received 1 November 2016; Accepted 4 January 2017; Published 1 March 2017

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