Impact of interaction between aflatoxicosis and cecal coccidiosis on broiler chickens

Published on: 6/28/2016
Author/s :

An experiment was conducted to evaluate the effect of dietary aflatoxin on broiler chicks infected with Eimeria tenella in a battery trial. A total of 120 broiler chicks were raised from one day to 35 days of age. Chicks were assigned into 4 experimental groups. The 1st group was infected with 5x104 sporulated oocysts of Eimeria tenella/ chick. The 2nd group received a combination of E. tenella infection and dietary aflatoxin (200 ppb). The 3rd group received dietary aflatoxin alone. The 4th group was kept as control.


The combination of aflatoxin and E.tenella caused higher mortality rate than aflatoxicosis and coccidiosis alone. Final body weight and feed conversion ratio deteriorated in all treated groups. Lesion scores and oocyst output were not significantly different in the 1st and 2nd groups. The highest levels of liver function enzymes, ALT (alanine aminotransferase) and ALP (Alkaline phosphatase) were observed in the Eimeria- aflatoxin treated group. Hemoglobin concentration and packed cell volume were significantly decreased in the 1st and 2nd groups. Histopathological examination revealed that the lesions were more pronounced in Eimeria-aflatoxin treated group, particularly in the liver. Cecal lesions were severe in the 1st and 2nd groups. Bursa and thymus revealed alterations in the 2nd and 3rd groups which were indicative of deleterious effect on the immune system of birds. The results indicated that combination of E. tenella infection and aflatoxicosis in broiler chickens may exaggerate the course of coccidial infection.



Intensive breeding farms enhance the simultaneous occurrence of several affections. Coccidiosis is a disease of greater economic importance and affections coexist with it should be considered. Among these affections, aflatoxicosis, which have been reported to be immunosuppressive (Bakshi et al., 2000) leading to an increase in the susceptibility of chickens to avian pathogens including coccidiosis (Pier et al., 1972, Richard et al., 1973, Edds and Bortell, 1983, Saif, 2003).


Aflatoxicosis in broiler chickens has been widely investigated by the determination of their growth inhibitory effects (Oguz and Kurtoglu, 2000c). The biochemical–hematological (Oguz et al., 2000a), immunological (Qureshi et al., 1998) and pathological toxic effects of Aflatoxin (AF) have also been well described (Dafalla et al., 1987; Kiran et al., 1998).


Although the most important toxicological target of AF in chickens is the liver, the descriptions of the clinical, pathological and biochemical findings vary considerably especially if another disease arises along with it (Stoev et al., 2002). So it is important to understand the complicated clinicopathological findings of such case.


The aim of this study was to investigate the influence of interaction between dietary aflatoxin and Eimeria tenella infection in broiler chickens.


Material and methods

Parasite samples:

A field isolate of E. tenella, obtained from a previous study by Abuakkada and Ellakany (2008) from a broiler farm suffering from bloody diarrhea and daily mortality, was used for the experimental infection. This isolate was identified, purified and propagated according to Davies et al. (1963). The pathogenicity and the infective dose of the isolate were determined. The infective dose used for the experimental infection was 50,000 oocyst / chick.


Production of aflatoxin:

Aflatoxin was produced by growing standard aflatoxigenic strain on sterile polished rice by the method of Shotwell et al. (1966) and modified by West et al. (1973). Briefly, rice was cleaned, washed and autoclaved at 121 C for 15 minutes, dispensed in 500 ml Earlynmyer flasks and moistened by distilled water (10 ml/flask). Each flask was injected by 10 ml of fresh saline spore suspension of Aspergillus flavus containing 108 spores/ml, and then sealed by tight cotton cork. Flasks were incubated for 2 days at 18 C, then for other 5 days at 26 C. The flasks were shaken vigorously everyday to prevent clumping of the rice, to ensure a homogenous toxin distribution and to prevent the fungal overgrowth. Finally, the flasks were sterilized by autoclaving to kill the fungus and its spores, while toxins were restored. The rice thereafter was  dried, ground in an electric blender until being powder.


Detection of aflatoxin:

Aflatoxin was detected quantitatively by using affinity column chromatography (Aflatest 10, Naremco, Springfield, USA) and flurometer (Sequcia Tuner Model 450 with 360 nm excitation filter and 450 nm emission filter) by the method of Nabney and Nesbitt(1975).


Experimental animals:

A total of 120, one-day-old un-sexed, Hubbard broiler chicks were reared for 5 weeks on a wire floor electric starter batteries where feed and water were supplied without restriction. They were fed a commercial broiler home made starter ration free from anticoccidial drugs.


Experimental design:

On the 7th day of age, all birds were weighed and allocated into 4 main groups (30 birds each) each main group included 3 replicates (10 chicks each). They were ranked by the Restricted Randomization Procedure that approximately equalized the initial body weights among the different groups. The 1st group was infected with 5x104 sporulated oocysts of Eimeria tenella/ chick. The 2nd group received a combination of E. tenella infection and dietary aflatoxin (200 ppb). The 3rd group received dietary aflatoxin alone (200 ppb). The 4th group was kept as control. Before infection, fecal samples from all birds were examined microscopically to prove that they were free from coccidial infection.


All birds were individually weighed weekly starting from 7th day of age until the end of the experiment. Chicks were infected with E.tenella sporulated oocysts on 14th days of age by direct inoculation into the crop using an insulin syringe. Intoxicated feed was supplied to birds of the 2nd and 3rd groups form 7th day of age until 2 weeks before the end of the experiment.


Parameters of evaluation:

Performance traits included body weight (BW), BW gain, feed consumption, feed conversion ratio (FCR), mortality, post-mortem examination, lesion scoring, oocyst count, histopathological examination, hematological and biochemical parameters were evaluated.


Oocyst count:

Oocyst count per gram fecal material (OPG) was evaluated from the 7th to 14th days post- infection (PI). Three samples representing each group were examined and OPG were counted using Mac Master counting technique according to Long and Joyner (1976).


Lesion scores:

Lesion scores of E. tenella were evaluated according to Johnson and Reid (1970) 5 days PI. Three birds from each group were sacrificed and cecal lesions were scored as follows:

  • Score 1: few scattered petechiae on the cecal wall.
  • Score 2: noticeable blood in the cecal contents, with thickened cecal wall.
  • Score 3: blood or cecal cores and severely thickened cecal wall.
  • Score 4: cecal wall is severely distended with caseous bloody cores and the bird is dead.


Hematological and biochemical parameters:

Blood samples were collected from all groups on the 5th day PI. They were used for determination of packed cell volume (PCV) according to Jaine (1993) and estimation of Hemoglobin concentration (Hb) according to Drabkin (1949). For biochemical analysis, blood samples were used for serum separation and evaluation of liver function tests, ALT (alanine aminotransferase) and ALP (Alkaline phosphatase) activities using commercial kits supplied from Biomerieux (France) according to Brugere-Picoux et al. (1987). Albumin determination was done according to Varely et al. (1980). Differential leukocytic counts were performed using an improved Neubaur hemocytometer. Percentage of each type of white cells was calculated according to Hawk (1965).


Histopathological examination:

From those birds examined for lesion scores, 5 days PI, cecal parts as well as specimens from liver, bursa and thymus were collected, immediately fixed in 10% neutral buffered formalin, processed through the conventional paraffin embedding technique, sectioned and stained with haematoxylin and eosin (H&E) for the histopathological examination according to Culling (1983).


Statistical analysis:

Data obtained were compared using the General Linear Models (GLM) procedure and least squares means of SAS® (SAS Institute, 1989).



Table (1) shows that E. tenella and aflatoxin-treated birds had significantly higher number of oocysts on the 7th, 11th and 14th days PI compared to the group infected with Eimeria tenella alone. However, total oocyst count showed no significant difference between both groups. Aflatoxin-treated and control groups were negative for E.tenella oocysts throughout the experiment.


Table (2) shows that the highest mortality rate was observed in the group treated dually with aflatoxin and E. tenella (20%) followed by the group treated with E. tenella alone (13.3%), then the aflatoxin-treated group (10%). Lesion scores of chickens 5 days PI with E. tenella did not differ significantly between groups infected with E. tenella or in combination with aflatoxins.


Growth and FCR presented in Table (3). There was a significant reduction in the final BW in all treated groups compared to control group. The reduction was observed in the aflatoxin (1133.75 g) and E.tenella-aflatoxin (1172.22 g) treated groups followed by E.tenellainfected group (1354.29 g). Also, FCR of the group treated dually with E. tenella and aflatoxins was significantly the worst value of (2.02) compared to aflatoxin treated (1.93), E.tenella infected (1.84) and control (1.70) groups.


Results in Table (4) reveals significant reduction in PCV%, Hb content and blood lymphocyte% in E.tenella-aflatoxin-treated (26.67%, 17.90 g/dl and 42.50%, respectively), E. tenella-infected (25.33%, 18.13 g/dl and 42.50%, respectively) groups compared to control group (28.00%, 22 g/dl and 45.67%, respectively). On the other hand, the three hematological parameters of aflatoxin -treated group were (28.67%, 20.60 g/dl and 44.33%, respectively) compared to control.


Table (5) shows that aflatoxin alone or in combination with E. tenella caused a significant elevation in serum activity of ALT (178.22 and 181.11 U/L), ALP (412.96 and 422.46 U/L) and a reduction in serum albumin (1.75 and 1.72 g/dl) compared to the control values (135, 285 U/L and 2.08 g/dl). E.tenella alone induced a significant reduction in serum albumin level (1.86 g/dl).


Gross Pathology:

Liver of aflatoxin-treated and Eimeria-aflatoxin-treated groups was enlarged and yellow in color. The cecum of Eimeria-treated and Eimeriaaflatoxin- treated groups was enlarged and thickened with hemorrhagic contents besides congested and hemorrhagic mucosa. Atrophy of the bursa of Fabricious and thymus was noticed in aflatoxin-treated and Eimeria-aflatoxin-treated groups.



Liver of Eimeria-aflatoxin-treated group showed severe diffuse hepatocytic vacuolation (Fig.1) with presence of multifocal areas of coagulative necrosis infiltrated with mononuclear cells, primarily lymphocytes (Fig.2). Hyperplasia and desquamation of the biliary epithelium with periductal fibrosis and lymphocytic cell infiltrations were noticed (Fig.3). Similar lesions were observed in liver of aflatoxintreated group but less in severity than those of previously mentioned group. Severe cecal lesions were observed in both Eimeria-treated and Eimeria-aflatoxin-treated groups. These lesions consisted of severe mucosal and submucosal congestion, edema and hemorrhage (Fig.4) as well as mononuclear cell infiltrations, chiefly lymphocytes. In addition, the mucosal epithelium showed severe diffuse degeneration, necrosis and desquamation (Fig.5) besides presence of numerous numbers of intracellular developmental stages almost schizonts (oval structure containing basophilic banana-shaped merozoites, Fig.6). Cecum of aflatoxin-treated group showed mild degenerative and necrotic changes as well as desquamation of the mucosal epithelium (Fig.7). Lymphoid organs exhibited necrotic changes in aflatoxin-treated and Eimeria-aflatoxintreated groups, but were more severe in the latter. These changes were severe diffuse lymphocytic cell necrosis and depletion giving the bursal follicle moth-eaten appearance (Fig.8). Some bursal follicles showed large cystic cavitations devoid of lymphocytes and containing faint eosinophilic necrotic debris (Fig.9). Similar lesions were seen in the thymic follicles (Fig.10) besides interfollicular congestion.


Table (1): Effect of dietary aflatoxin and Eimeria tenella infection on mean oocyst count (103 per gram feces) from 7th – 14th day PI in broiler chickens.

PI, Post infection. AF, Aflatoxin. 
Values are means ± standard errors.
Means in the same row without a common letter differ significantly (P<0.05).


Table (2): Effect of dietary aflatoxin and Eimeria tenella infection on mortality and lesion scoring 5 days PI of broiler chickens.

Values are means ± standard errors.
Different small letters indicated that means of different groups are significantly different at (P < 0.05).


Table (3): Effect of dietary aflatoxin and Eimeria tenella infection on body weight (BW), BW gain and feed conversion ratio(FCR).

Values are means ± standard errors.
Different small letters indicated that means of different groups are significantly different at (P < 0.05).


Table (4): Effect of dietary aflatoxin and Eimeria tenella infection on hematological parameters of broiler chickens.

Values are means ± standard errors.
Different small letters indicated that means of different groups are significantly different at (P < 0.05).

Table (5): Effect of dietary aflatoxin and Eimeria tenella infection on liver functions of broiler chickens.

Values are means ± standard errors.
Different small letters indicated that means of different groups are significantly different at (P < 0.05).


Fig. (1): Liver of an Eimeria-aflatoxintreated bird: Severe diffuse hepatocytic vacuolation (arrows). H&E(X400).   Fig. (2): Liver of an Eimeria-aflatoxintreated bird: Focal area of coagulative necrosis infiltrated with lymphocytes (arrow) as well as hepatocytic vacuolation. H&E(X400).
Fig. (3): Liver of an Eimeria-aflatoxin-treated bird: Hyperplasia and desquamation of biliary epithelium (arrow) with periductal fibrosis (star) and lymphocytic infiltration (arrowheads). H&E(X100).   Fig. (4): Cecum of an Eimeria-aflatoxin-treated bird: Severe submucosal hemorrhage (A) and edema (B) with necrotic desquamated mucosal epithelium (star) and presence of intracellular developmental stages of Eimeria tenella (arrows). H&E(X100).
Fig. (5): Cecum of an Eimeria-aflatoxin-treated bird: Severe necrosis and desquamation of the mucosal epithelium that completely replaced by schizonts (A) besides submucosal hemorrhage (B). H&E(X100).   Fig. (6): Cecum of an Eimeria-aflatoxin-treated bird: Numerous intracellular schizonts containing banana-shaped merozoites (arrows) with severe mucosal and submucosal hemorrhage (A) and focal lymphocytic infiltration (arrowhead). H&E(X400).
Fig. (7): Cecum of an aflatoxin-treated bird: Mild necrosis and desquamation of the mucosal epithelium (arrow). H&E(X100).   Fig. (8): Bursa of Fabricious of an Eimeriaaflatoxin- treated bird: Severe diffuse lymphocytic cell necrosis and depletion represented by empty spaces (arrows). H&E (X400). 
Fig. (9): Bursa of Fabricious of an Eimeriaaflatoxin- treated bird: Large cystic cavitation in a bursal follicle containing faint eosinop- hilic necrotic debris (arrow) and slight lymphocytic cell depletion in others (arrowheads). H&E(X100).   Fig. (10): Thymus of an Eimeria-aflatoxin-treated bird: Lymphocytic cell necrosis and depletion represented by empty spaces (arrows). H&E(X400).



Coccidiosis is one of the most important causes of economic losses in poultry industry (Williams et al., 1999). Eimeria tenella is a pathogenic species infecting chickens. Economic losses are primarily due to impaired feed conversion, depressed growth and mortality (Tipu etal. 2002). Profitability of poultry production can be greatly affected due to frequent feed contamination with AF and their detrimental effects on the performance (Hamilton, 1984). In chickens, aflatoxin increases the susceptibility to, or severity of, cecal coccidiosis, Marek’s disease, salmonellosis, inclusion body hepatitis and infectious bursal disease virus (Saif, 2003). Increased susceptibility of aflatoxicated chicks to infectious diseases indicates impaired immune responses (Bakshi et al., 2000) and breakdown of vaccinal immunity (Panisup et al., 1982).


As a general rule, growing poultry should not receive more than 20 μg of aflatoxin in the diet (Celyk, etal., 2003). Several studies in the Egyptian field tested rations and feed ingredients and proved their contamination with more than the allowed level of mycotoxins (Ellakany, 1991 and Gamal Aldeen, 2001).


This study indicated that AF may complicate the clinical picture of cecal coccidiois. Wherein, the impairments in the performance traits including body weight, body weight gain, feed conversion ratio (FCR), mortality rates as well as histopathological and biochemical alterations were intensified when chicks received a combination of aflatoxin and E. tenella infection.


Aflatoxin in ration alone or combined with E.tenella infection caused significant depression in average body weight when compared to non- infected control group. The growth depression and poor FCR may be due to anorexia, listlessness and the inhibitory effect of aflatoxin on the protein synthesis and lipogenesis (Oguz and Kurtoglu, 2000c). These results were in agreement with other reports of aflatoxin studies (Stewart et al., 1998, Allameh et al., 2005).


Regarding oocyst count and lesion scores, data showed that there was no signinficant difference between chickens received AF and E. tenella together and chickens infected with E. tenella alone. This may be due to that AF did not interfere with the developmental stages of E.tenella in broiler chickens. Similar results were recorded by Shakshouk et al.(1991).


Concerning mortality, results indicated that simultaneous aflatoxicosis and cecal coccidiosis caused higher mortality than either aflatoxicosis or cecal coccidiosis alone. These results confirmed previous findings that AF in the feed of chickens can increase the susceptibility of the host to parasitic diseases (Wyatt et al., 1975 and Shakshouk et al., 1991) and additionally indicated that subclinical coccidiosis may be accentuated by dietary aflatoxin. Increased mortality rates may be due to the immunosuppression induced by AF in diet. This was supported by the findings of pier et al (1972), Wyatt et al (1975) and Giambrone et al (1978).


The observed significant reduction in Hb and PCV values in E.tenella-infected-aflatoxin- treated group confirmed the earlier findings of Doerr and Huff (1980), Singh et al. (1992) and Mani et al. (1993). The reduction in Hb and PCV values observed during aflatoxicosis may be due to reduced protein synthesis (Sakhare, etal., 2007) resulted from aflatoxin provoked liver damage. Lymphocytic count was significantly decreased in all treated gropups in comparison with control group indicating depression of cell mediated immunity caused by both aflatoxin (Bakshi et al., 2000) and cecal coccidiosis (Lillehoj and Trout, 1993).


Moreover, significant increase in ALP and ALT serum levels was observed in E. tenella-aflatoxin-treated and aflatoxin-treated groups as a sequel of aflatoxin action. This could be attributed to the clear damage in the liver, particularly the bile ducts resulting in increased release of functional enzymes from the biomembranes. Marked significant reduction of serum albumin level was observed in the groups which received AF alone or a combination of AF and E.tenella infection compared to other groups. These biochemical findings are in agreement with Kalorey (1993) and Sakhare, etal., (2007).


Liver and the immune system organs (bursa and thymus) are considered to be target organs for AF (Ortatatli et al., 2005). Aflatoxininduced immunosuppression was explained by atrophy of the bursa of Fabricius and thymus (Saif, 2003). In addition, aflatoxin induced hepatic lesions consisted of bile duct hyperplasia and fatty changes which could be ascribed either to general inhibition of lipid transport (Tung, etal. 1972) or to interference with lipogenesis (Donaldson, etal. 1972). Similar pathological findings in the liver of broilers with aflatoxicosis were reported by Ortatatli and Oguz (2001) and Safameher (2008). These alterations were more pronounced in Eimeria-aflatoxin-treated group. Furthermore, cecal lesions were severe in both Eimeria-treated and Eimeria-aflatoxin-treated groups. Similar results were proved by Stoev, etal.(2002).


It could be concluded that aflatoxicosis in association with cecal coccidiosis may complicate the clinicopathological findings of such case resulting in enormous economic losses.



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Head of Poultry Diseases Dept. at Damanhour University, Vice Dean for Education and Student Affairs at Faculty of Veterinary Medicine.
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