Indian Journal of Animal Research

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Research Article

Indian Journal of Animal Research, volume 55 issue 6 (june 2021) : 704-709

Performance, Immune Response and Blood Biochemical Traits of Broiler Chickens Fed Graded Levels of Dietary Aflatoxin and Ochratoxin Combination

T. Tamilmani1, Avishek Biswas1,*, Asitbaran Mandal1
1Avian Nutrition and Feed Technology Division, ICAR-Central Avian Research Institute, Izatnagar-243 122, Uttar Pardesh, India.
Cite article:- Tamilmani T., Biswas Avishek, Mandal Asitbaran (2020). Performance, Immune Response and Blood Biochemical Traits of Broiler Chickens Fed Graded Levels of Dietary Aflatoxin and Ochratoxin Combination . Indian Journal of Animal Research. 55(6): 704-709. doi: 10.18805/IJAR.B-4003.

ABSTRACT

Background: Feed quality in terms of nutritional content is plays pivotal role in achieving desired production. Amongst the several factors which alter the quality of feed, inevitable fungal toxins that compromise the nutritive content quite often had taken attention posing serious health hazards on birds and humans as well. Moulds / Fungi are accomplished of reducing the nutritional value of feedstuffs as well as expanding some mycotoxins. Mycotoxin adulterated feed has adverse effects on poultry health and productivity. The present study aimed to study the effect of dietary supplementation of graded levels of dietary aflatoxin and ochratoxin combination on performance, immune response and blood biochemical traits of broiler chickens. 

Methods: A 42 days biological trial was conducted to study the effect of graded levels of aflatoxin B1 (AFB1) and ochratoxin (OTA) combination in the diet for production, immune response and blood biochemical parameters of broiler chickens. Day-old broiler chicks (n=240) were divided into five (5) treatment groups (T1: control; T2: T1 + 100 ppb AFB1+ 100 ppb OTA; T3: T1 + 100 ppb AFB1+ 200 ppb OTA; T4:T1 + 250 ppb AFB1+ 100 ppb OTA; and T5: T1 + 250 ppb AFB1+ 200 ppb OTA) and each treatment was fed to 6 replicated groups of 8 birds each. 

Result: Body weight gain (BWG) was significantly lower in T3, T4 and T5 group and feed intake (FI) in all the toxin supplemented groups was statistically similar but numerically higher compared to control group. Significantly lower feed conversion ratio (FCR) was recorded in 0-42 d at T1 and T2 group. The cell mediated immunity (CMI) and humoral immunity (haem-agglutination- HA titre) in higher doses of aflatoxin and ochratoxin combined fed group (T5) was lower (P<0.05). The liver damage enzymes such as alanine aminotransferase (ALT) and alkaline phosphatase (ALP) were increased (P<0.05) in broilers fed on diet containing aflatoxin and ochratoxin combinations. Significant (P<0.05) reduction in serum uric acid and cholesterol level at T3, T4 and T5 dietary treated groups. No significant (P>0.05) changes observed in total protein and aspartate aminotransferase (AST) concentration.  Thus, it may be concluded that combination of Aflatoxin B1 (100 ppb) and ochratoxin A (100 ppb) in basal diet had no adverse effect on growth performance, immune response and blood biochemical parameters in broiler chicken.

INTRODUCTION

Poultry production is one of the fastest growing segments of the agricultural sector in India with rising rate of 10% per annum and it is the major contributor to growing economy of the country. Currently, the total poultry population in India is 729.21 million (as per 19th Livestock Census) and the egg production has increased from around 83 billion nos. in 2015-16 to around 88 billion in 2016-17 registering a growth of about 6% (DAHDF, 2017). In recent years, health hazards due to mycotoxins are posing a major threat to the poultry industry. Food grains getting damaged are common in India due to poor handling and storage facilities, high temperature and humidity. Mycotoxin contamination in the feed is a worldwide problem. FAO (2004) has estimated that up to 25% of the world’s food cereals and a higher percentage of the world’s animal feedstuffs are significantly contaminated by mycotoxins. Mycotoxins are a group of structurally diverse secondary metabolites of fungi that occur as contaminants of grains worldwide. Aspergillus, Alternaria, Claviceps, Fusarium and Penicillium species of fungi are ubiquitous in nature and under ideal conditions often infect economically important crops during storage, shipment and processing.
               
Aflatoxins (AFB1) and ochratoxins (OTA) are the toxic compounds produced by various species of ubiquitous genera, Aspergillus and Penicillium. The toxicopathological spectrum of AFB1 and OTA is very wide, encompassing different kinds of toxicities as acute, chronic, carcinogenicity, teratogenicity and immunotoxicity (Huff et al., 1984). AFB1 is primarily hepatotoxic, whereas OTA is primarily nephrotoxic.
They have significant impact on economic returns due to decreased productivity, immunosuppression and increased mortality due to secondary infections fungal contamination of agricultural products and also the poultry feed is often unavoidable and is of worldwide concern (Khan et al., 2013). The quality of feed plays an important role in the performance of broilers. Dual occurrence of aflatoxin and ochratoxin in poultry diets is a severe threat as they interact synergistically to become more toxic when they occur as simultaneous contaminants of poultry diet (Huwig et al., 2001).
       
Keeping in view the above facts, the objective of the present study was to determine the effects of graded levels of dietary aflatoxin and ochratoxin combinations on performance, immune response and different organ weight of broiler chickens.

MATERIALS AND METHODS

All animal studies were conducted in accordance with recommendations described in ‘Institutional Animal Ethics Committee (IAEC, CARI, Izatnagar)’.
 
Aflatoxin production
 
Lyophilized preparation of Aspergillus parasiticus NRRL 2999 was obtained from U.S. Department of Agriculture, Peoria, Illinois (USA). The lyophilized preparation was revived on potato dextrose agar (PDA) medium and used for aflatoxin (AF) production by fermentation of cracked maize as per Shotwell et al., (1966). The fermented maize was steamed to kill the fungus spores, dried and ground to a fine powder. The aflatoxin concentration from maize powder was extracted as per Pons et al., (1966) and measured using thin layer chromatography (TLC). The total AF concentration in maize powder consisted of 77.46% AFB1, 11.73% AFB2, and 8.28% AFG1 and 2.53% AFG2. The maize powder containing known concentration of AF was incorporated into the basal diets of certain dietary treatments to get the desired amount of one (1) ppm total AF.
 
Ochratoxin production
 
The lyophilised preparation of Aspergillus westerdijkiae NRRL 3147 was obtained from U.S. Department of Agriculture, Peoria, Illinois (USA). This lyophilised preparation was revived on potato dextrose agar (PDA) medium and used for experimentation. Ochratoxin was produced as per the method described by Singh et al., (2013). Cracked maize (50 g) was taken in 250 ml conical flasks. The moisture content of substrate was adjusted of 35%. Thus flasks were plugged with non-absorbent cotton and sealed with aluminium foil. The flasks were autoclaved for 20 min at 120oC and inoculated with 1-week old spores of Aspergillus westerdijkiae NRRL 3174. The inoculated flasks were incubated in a incubator for 14 days. After removal from the incubator, the flasks were dried at 70oC and the ochratoxin assays were performed as per AOAC (1995).
 
Experimental birds, diets and management
 
The experiment was conducted at Avian Nutrition and Feed Technology division, ICAR-Central Avian Research Institute, Izatnagar, India on February-March, 2019. There were five dietary treatments and each dietary treatment had six replicates and each replicate had eight chicks (5 x 6 x 8 = 240). Experimental design was completely randomized design (CRD) and the experiment was conducted in broiler chickens from day-old to 42 day of age. The various dietary treatments were prepared by mixing the required quantity of mouldy maize to get the desired concentration of AFB1 and OTA in basal diet. Experimental diets included T1: control (basal diet), T2: (T1 + 100 ppb AFB1+ 100 ppb OTA), T3: (T1 + 100 ppb AFB1+ 200 ppb OTA), T4: (T1 + 250 ppb AFB1+ 100 ppb OTA), and T5: (T1 + 250 ppb AFB1+ 200 ppb OTA). Day-old broiler chicks (n=240) were obtained from experimental hatchery, Central Avian Research Institute (CARI), Izatnagar, India. The chicks were wing banded, weighed individually and distributed randomly into five groups. All birds were reared under standard managemental conditions from 0-42 days. All birds were fed with broiler starter ration from 1-21 days and broiler finisher ration from 22 to 42 days. The basal diet (Table 1) was prepared using maize, soybean meal and rapeseed meal. The starter diet (0-21 days of age) contained 21.5% protein, 2,890 kcal ME/kg, lysine 1.28%, methionine 0.52%, calcium 1.02% and available P 0.45%. The corresponding values in finisher diet were 19.02%, 29,991 kcal/kg and 0.93%, 0.39%, 1.09% and 0.39%.
 

Table 1: Ingredient and chemical composition of basal feed.


 
Production performance
 
Body weight gains (BWG) were recorded during the experimental period to ascertain the 0-3 and overall body weight gain. A weighed quantity of respective diet was offered ad lib daily to each groups of each dietary regimen in the morning and the residue was weighed next day on daily basis in order to arrive at overall feed intake. Based on the data pertaining to the feed intake (FI) and BWG, the weekly and period wise feed conversion ratio (FCR) of birds was determined. Daily monitoring and recording on individual basis were carried out to study the mortality of the experimental birds used in the present investigation. Mortality was measured when occurred.
 
Immune response
 
Ten birds were selected from each of the treatment group (n= 50) at 28 d of age and were inoculated intravenously with 1.0 ml of 1% suspension of sheep red blood cells (SRBC) to investigate the effect on the humoral immune response. Blood samples were obtained from the jugular vein from all SRBC injected birds at 0 and 6 d post-inoculation. All the samples were incubated at 37oC for one hour to aid clotting and retraction then centrifuged at 1512 g for 5 min for collection of sera. All the microtitre plates (U-bottomed) were rinsed with 50μl of phosphate-buffered saline (PBS; pH 7.6), 50μl of sera was added in first well and 50ìl of 1% SRBC in PBS was added in each well then dried before the haem agglutination antibody (HA) titre was estimated by a micro-haem agglutination method (Siegel and Gross, 1980) using two-fold serial dilutions of sera.The foot web index (FWI) was used as an index of the cell-mediated immune response at 35 d of age. Ten separate birds from each replicate of the prebiotics treatment groups were selected and 0.2 ml PHA-P mitogen (1 mg/ml PBS) was injected intra-dermally into the left foot web. Sterile PBS (0.2 ml) was injected into the right foot web to serve as a control. A micrometer was used to measure changes in the thickness of both foot webs. Measurements were made at 0 and 24 h after the injection, as described by Cheng and Lamont (1988). Foot web swelling was calculated by subtracting skin thickness at 24 h post-injection from that at 0 h pre-injection.
 
Blood biochemical parameters
 
At the end of the feeding trial (42 d), 2 ml of whole blood was collected from the wing vein from each bird (n=10/group) into sterile glass tubes without anticoagulant. Test tubes containing the blood were kept in slanted position at room temperature for half an hour to facilitate separation of serum. Serum was separated by centrifugation at 1512 g for 10 minutes and decanted into plastic vials and then stored at -20oC for estimation of alkaline phosphatase (ALP), aspartate aminotransferase (AST), alanine aminotransferase (ALT), uric acid, total protein and total cholesterol. All blood biochemical parameters were measured based on spectrophotometric assays using commercially available diagnostic kits (Span Diagnostics, India).
 
Statistical analysis
 
Data were statistically analysed with version 20.0 SPSS software (SPSS, Chicago) using one way ANOVA. Duncan’s (1955) multiple range test was used to compare means of different experimental groups. Significant statistical difference was assumed at the level of P < 0.05.

RESULTS AND DISCUSSION

Production performance
 
Significant (P<0.05) differences in body weight gain (BWG) among various treatments were observed 21-42 d and overall growth phase (0-42 d of age), where in the BWG in T5 was lower (P<0.05) than that of control group (T1), however, the BWG in T2, T3 and T4 was statistically similar to that of control (Table 2). These results were in agreement with earlier workers who reported significant reduction in BWG after dietary supplementation of aflatoxin or ochratoxin (El-Barkouky, 2008, Hanif et al., 2008 and Elaroussi et al., 2008). In the present study, addition of 100 ppb AFB1 with 100 ppb OTA in basal diet did not produce any significant change in BWG of broiler chicks, indicating that broilers can tolerate up to 100 AFB1 with 100 ppb OTA in their diet. Pozzo et al., (2013) also reported that feeding broiler chickens, a diet contaminated with 100 ppb OTA or 100 AFB1 did not affect any weight gain of broiler chickens. Feed intake (FI) of the present study was statistically similar to that of control (T1); however, the feed consumption of groups T3, T4 and T5 was numerically lower than that of control group. The results of the present study are not in agreement with earlier workers who reported significant reduction in FI at 200 to 800 ppb level of dietary ochratoxin (Hanif et al., 2008, Santin et al., 2003).
 

Table 2: Effect of varying levels of dietary aflatoxin and ochratoxin combinations on production performance in broiler chickens (0-42days).


       
Significant (P<0.05) differences in feed conversion ratio (FCR) among various dietary treatments were recorded in overall growth phases (0-42 d of age). The FCR of other two phases (0-21 and 21-42 d) were statistically similar to that of control (T1). Similar observations of reduced feed efficiency were also made by earlier workers (El-Barkouky, 2008, Hanif et al., 2008). In the present study, addition of 100 ppb of each i.e., AFB1 and OTA in the diet did not bring out any significant change in FCR of broiler chickens.
 
The mortality percentage was not affected in basal diet and basal diet with 100 ppb OTA and 100 ppb AFB1. However, the moratlity percentage increased at AFB1 and OTA levels at 200 ppb level. However, El-Barkouky and Abu-Taleb (2008) reported that contamination of broiler diet with AFB1 with OTA at 200 ppb each resulted in a significant increase in mortality rate of broilers. Increased mortality due to mycotoxicosis in poultry was also reported by Singh et al., (2017). The results of the present study showed that broiler chicken can tolerate 100 ppb AFB1 with 100 ppb of OTA in their diet without any adverse effect on survivability.
Immune response
 
The data pertaining to cell mediated immunity (CMI) response to PHA-P measured as foot web index and humoral immune response measured as haem-agglutination titre (HA) against sheep red blood cells (SRBC) in broiler chickens fed various dietary treatments is presented in Table 3. The CMI value of control group (T1) and T2 was higher (P<0.05) than that other dietary mycotoxin fed groups (T3, T4 and T5). The results revealed that contamination of dietary combination of aflatoxin and ochratoxin in feed reduced (P<0.05) the CMI response as compared to that of control (T1). The CMI value in T2 was statistically similar to that of control, indicating that the addition of 100 ppb Aflatoxin and 100 ppb ochratoxin to the basal feed did not produce any effect on CMI response. Singh et al., (2013) showed suppression of CMI response in chicken due to ochratoxicosis and described the significant reduction of T-lymphocyte count and phagocytic ability of spleenic macrophages after feeding 0.5 and 2.0 ppm ochratoxin. These findings were also supported by Verma et al., (2004) in broilers fed with 1-4 ppm ochratoxin for 47 days from one day of age. Reduction in CMI response was also observed by Wang et al., (2009).
 

Table 3: Effect of varying levels of dietary aflatoxin and ochratoxin combinations on immunity blood biochemical parameters in broilers chicken (N = 40).


       
The HA titre value in ochratoxin and aflatoxin (100 ppb each) fed group (T2) was statistically similar to that of control (T1). The HA titre value of T3, T4 and T5 was statistically similar. In the present study, dietary higher doses of aflatoxin and ochratoxin combination reduced (P<0.05) the HA titre against sheep RBC’s. Combination of aflatoxin and ochratoxin interferes with protein, DNA and RNA synthesis through competitive inhibition of phenylalanine-t-RNA syntheses by phenylalanine moiety of mycotoxin that leads to decrease plasma proteins and immunoglobulin (Marquardt and Frohlich, 1992). El-Barkouky (2008) also found that inclusion of higher doses of aflatoxin and ochratoxin combination deteriorates the humoral immune response.
 
Biochemical parameters
 
The impact of probiotic supplement during broilers on serum biochemical parameters has been summarized in Table 3. The levels of liver damage enzymes such as alanine amino transferase (ALT) and alkaline phosphatase (ALP) determined measured at the end of growing period were increased (P<0.05) in broilers fed on diet containing aflatoxin and ochratoxin combinations. This finding was more obvious with the experimental group fed high dose aflatoxin (200 ppb) and ochratoxin (200 ppb) i.e., T5 group. The present finding are in agreement with the findings of Hanif et al., (2008) who reported that increased ALT and ALP due to mycotoxicosis in broiler chickens. In the present study, there was a significant (P<0.05) reduction in serum cholesterol level at T3, T4 and T5 dietary treated groups in compared with control group. Mycotoxins reduced (P<0.05) the concentrations of uric acid and cholesterol concentration compared with those of the control groups. In respect of serum cholesterol during ochratoxicosis, a similar trend was reported earlier by Ramadevi et al., (2000) and Stoev et al., (2000). In the present study, there was a significant decrease in serum uric acid level in T3, T4 and T5 group where more dietary combination of AFB1 and OTA added.  The decrease observed in uric acid levels can be explained by changes in the efficiency of amino acid utilization, in enzyme systems, in renal filtration, or in reabsorption rates or by unknown aspects (Swamy et al., 2003). The transport and plasma profile of lipids may also be influenced by liver damage caused by mycotoxins, particularly aflatoxins or ochratoxins. Thus, serum cholesterol reduction caused by mycotoxin can be related to inhibition of the biosynthesis of the compound to liver damage and changes in concentration of circulating cholesterol to the liver (Kubena et al., 1988).

There were no significant (P>0.05) changes observed in total protein and AST concentration among the control and mycotoxin supplemented groups. The present findings are not in agreement with Safameher (2008) and Allameh (2005), who reported significantly decreased serum proteins and increased the AST during induced mycotoxicosis in broiler chickens after supplementation of AFB1 and OTA in diet. Results of the present study and those cited appear to justify the conclusion by Oguz et al., (2002) that supplementation of dietary concentrations of AFB1 and OTA cannot alter the serum total proteins. In case of other species turkey poult’s observed a reduction in serum total proteins in the groups fed AFB1 alone and in combination with OTA (Weibking et al., 1994). In the present study, addition of 100 ppb OTA and 100 ppb AFB1 in basal diet did not harvest any change in biochemical parameters. These results were in agreement with earlier report of Pozzo et al., (2013) who reported that 100 ppb dietary OTA or 100 ppb AFB1 did not alter biochemical parameters in broilers.
 
It was concluded that broiler chicken can tolerate a combination of 100 ppb ochratoxin with 100 ppb aflatoxin and have shown any adverse effects on their performance, immunity and biochemical parameters in broiler chickens; however, further study of this problem is required for confirmed.

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