Correlation incidence between infectious bursal disease and aflatoxicosis in broilers chicken farms in Nineveh province, Iraq
Iraqi Journal of Veterinary Sciences,
2023, Volume 37, Issue 1, Pages 183-190
10.33899/ijvs.2022.133881.2315
Abstract
This study aimed to investigate the incidence of infectious bursal disease IBD and aflatoxicosis with the correlation between them in broilers of six different areas in Nineveh Province, Iraq, which include: Mosul, Talafer, Hamdanya, Bartella, Baaj, and Gayara for six months (October 2021-March 2022). The necropsy of the suspected infected birds and blood sampling were conducted on 25 birds for each area to diagnose IBD. Samples of broiler feed were collected from the same farms to diagnose aflatoxin B1. The detection of both IBD and aflatoxicosis occurred by the ELISA technique. The necropsy results showed hydropericardium, paleness or congestion, friable and swelling of the liver, kidneys, and bursa of Fabricius, with more severe lesions in a few sporadic cases as gelatinous fluid surrounding the heart, intense paleness of the liver, kidney, and enlarged bursa of Fabricius. The detection of IBD revealed that the positive results were 142, and the negative results are 8 birds out of a total of 150 suspected broiler attributed to the subclinical infection according to the vaccine index equation. Also, positive aflatoxin B1 concentrations were recorded in all broiler feed in the 6 areas as the highest concentration mean was 0.23 ppb and the lowest concentration mean was 0.186 ppb in Mosul and Baaj, respectively. This study indicated a positive correlation between IBD and aflatoxin B1 but was not statistically significant.Introduction
Infectious bursal disease IBD or Gumboro disease as a synonym is an acute, highly contagious viral infection of young chickens 3 weeks of age and older that has lymphoid tissue, especially the bursa of Fabricious, as its primary target, and it is referred to as avian nephrosis because of the extreme kidney damage found in birds that succumbed to infection (1-3). The economic importance of this disease is the high mortality rate for some of its viral strains, which may reach 60% first. The second more critical manifestation is severe prolonged immunosuppression of chickens infected early or may not be clinically detectable (subclinical) (4,5). Sequelae related to this immunosuppression include hydropericardium hepatitis syndrome, anemic syndrome, E. coli infection, and vaccination failure. This is usually accomplished by combining maternal antibody transfer and active immunization of the newly hatched chick. The pathological changes in the bursa of Fabricious are enlargement, hemorrhage, and serous transudate. Also, hemorrhages and necrosis may be seen in the spleen, muscles, kidney, and intestines (6,7). Among the identified mycotoxins, aflatoxins primarily produced by Aspergillus flavus and Aspergillus parasiticus have received global concern because of their high toxicity and carcinogenicity (8,9). Predominately, aflatoxin B1 has potent carcinogenesis characteristics to the liver and other toxic effects, including immunosuppression, reduced protein synthesis, teratogenesis, and mutagenesis (10,11). The metabolism of aflatoxins is in the liver, so it exposes to injuries mostly. Aflatoxins also cause decreased egg production, hatchability, male and female fertility, and feed conversion efficiency (12,13). The pathological changes in the liver are redness due to congestion and hemorrhages with necrosis or yellowish due to fatty changes in addition to hemorrhages in other tissues (14). If the birds are fed aflatoxin with IBD virus infection, it reveals extensive symptoms and increased mortality (15). Aflatoxicosis increases the effects of IBD; therefore, the combination of both diseases offers a valuable potential model for understanding the correspondence between aflatoxicosis and infectious agents (16,17).
This study aims to detect the infectious bursal disease and aflatoxicosis in the broiler farms of six different areas in Nineveh province with the correlation incidence between the two diseases.
Material and methods
The study was designed to investigate and diagnose the infectious bursal disease and aflatoxicosis in broilers (3-5 weeks old) of six different areas in Nineveh Province, Iraq, consisting of Mosul, Talafer, Hamdanya, Bartella, Baaj, and Gayara for six months (October 2021-March 2022). The study parameters included:
Ethical approve OR data collection permit
The samples of the infected broiler with IBD and aflatoxicosis were obtained from the private broiler chicken farms located in the Mosul, Talafer, Hamdanya, Bartella, Baaj, and Gayara for six months in in Nineveh province, Iraq from October 2021to March 2022. It depends upon the submission of the College of Veterinary Medicine at the University of Mosul on form UM.VET.2021.44.
Necropsy examination
Necropsy examination of the recently dead chicks with clinical signs of IBD and aflatoxicosis was carried out, and the gross pathological findings were recorded. Representative tissue samples such as heart and liver were collected (18).
Blood samples:
One hundred fifty blood samples from infected chicken were collected from 6 broiler farms as 25 blood samples from each area, and the serum was separated from blood by centrifugation and stored at -20ºC to diagnose IBD by ELISA technique (19).
Feed samples
Twenty-four feed samples were collected from that 6 areas in Nineveh province as 2 feed samples from each farm to diagnose aflatoxicosis by ELISA technique.
Diagnosis of IBD by ELISA technique
It was measured by an ELISA kit manufactured by Bio check Co., Netherlands. Two plates were used to test 150 chicken serum samples. The technique principle depends on the detection of IBD virus antibodies in the serum by binding to the kit antigen, and the intensity of the color is measured by the amount of IBD antibody present in the test sample. The kit results suggest revealing the clinical infection, sub-clinical infection, or vaccination, which is measured by calculations and the following equation (vaccine index):SD (standard deviation)*100/ mean)*2.
Diagnosis of aflatoxicosis by ELISA technique
The technique principle is competitive ELISA for the diagnosis of aflatoxin B1. That aflatoxin antigen competes with the antigen in samples. The optical density OD value of the samples and the AFB1 concentration have a negative relationship, and the AFB1 concentration in the samples can be estimated by comparing the OD of the samples with the standard curve. The result is measured by calculations and equations attached to the kit.
Correlation between IBD and aflatoxicosis
A statistical program (SPSS software) was used to conduct the correlation analysis. Data were presented and analyzed using the Pearson correlation test with a significant level set on P<0.05.
Results
Necropsy examination
The results of necropsied birds showed the presence of serous transudate or fluid surrounding the heart (hydropericardium) with pale or congestion as mosaic appearance, friable and swelling of the liver (Figures 1 and 2). Moreover, there was swelling, paleness or necrosis, and congestion of the kidneys and bursa of Fabricious (Figures 3 and 4). There were more severe gross pathological changes in some sporadic birds’ cases of some broiler farms as intense paleness or fatty change of the liver with gelatinous fluid surrounding the heart (Figure 5) and severe swelling, paleness, icteric kidney and enlarged bursa of Fabricious surrounding by yellowish transudate and hemorrhage (Figure 6).
Figure 1: Cross section of broiler (3-5 weeks age) showing paleness and congestion as mosaic appearance and friable liver (arrow).
Figure 2: Cross section of broiler (3-5 weeks age) showing serous transudate or fluid surrounding the heart (black arrow) with congestion and swollen of the liver (yellow arrow).
Figure 3: Cross section of broiler (3-5 weeks age) showing swelling, paleness and congestion of the kidneys (yellow arrow) and bursa of Fabricious (black arrow).
Figure 4: Cross section of broiler (3-5 weeks age) showing mild enlarged and congestion of the kidneys (arrow).
Figure 5: Cross section of broiler (3-5 weeks age) showing severe paleness or fatty change of the liver (black arrow) and gelatinous fluid surrounding the heart (yellow arrow).
Figure 6: Cross section of broiler (3-5 weeks age) showing severe swelling, paleness, icteric kidney (yellow arrow) and enlarged bursa of Fabricious (black arrow) surrounding by yellowish transudate and hemorrhage (blue arrow).
Diagnosis of IBD by ELISA technique
The result revealed the titers of IBD antibody in the 6 areas of Nineveh Province, including Mosul, Talafer, Hamdanya, Bartella, Baaj, and Gayara as 2 broiler farms for each area with calculating the mean of each area, the positive results are 142 and the negative results are 8 of total 150 suspected broiler chicken. In order to find out the positive results, whether the result of a clinical or subclinical infection or from the vaccine, we applied the equation of the vaccine index. SD (standard deviation) *100 / mean)2) = (vaccine index) V.I. According to this equation and the kit’s instructions, if the vaccination index is more than 300, it results from clinical infection. If it is less, it is either the result of a subclinical infection or the IBD vaccine. Since there are no vaccination programs for IBD in poultry farms in the six study areas, the positive results are attributed to the presence of subclinical infection or a natural attack of the IBD virus (Table 1).
Table 1: The results of IBD diagnosis in the broiler chicken of 6 areas of Nineveh province by ELISA
Areas |
Farm (n) |
Samples (n) |
Farm (mean) |
Area (mean) |
Result of farms |
Infection type |
|||
- |
+ |
Clinical |
Sub-clinical |
vaccination |
|||||
Mosul |
1 |
14 |
4156.786 |
3518 |
1 |
13 |
- |
66.01 |
- |
2 |
11 |
2705 |
2 |
9 |
|||||
Talafer |
1 |
13 |
3886.76 |
4201.8 |
3 |
10 |
- |
81.09 |
- |
2 |
12 |
4543.08 |
Zero |
12 |
|||||
Hamdanya |
1 |
12 |
6255.917 |
3198.920 |
1 |
11 |
- |
63.57 |
- |
2 |
13 |
5543.538 |
Zero |
13 |
|||||
Bartella |
1 |
10 |
3185.4 |
4051.240 |
Zero |
10 |
- |
65.46 |
- |
2 |
15 |
3207.933 |
Zero |
15 |
|||||
Baaj |
1 |
14 |
3291.429 |
5885.480 |
Zero |
14 |
- |
244.78 |
- |
2 |
11 |
5018.237 |
Zero |
11 |
|||||
Gayara |
1 |
15 |
3172.386 |
2956.56 |
Zero |
15 |
- |
62.5 |
- |
2 |
10 |
2682 |
1 |
9 |
Diagnosis of the aflatoxicosis by ELISA technique
The result showed the positive results of aflatoxin B1 titers but less than the permissible limit of 20 ppb in all broiler feed samples of the broiler farms in the 6 areas as 2 feed samples for each farm and 2 farms for each area with a total of 24 feed samples. Mosul's highest mean titer of aflatoxin B1 was 0.23 ppb, and the lowest mean titer was 0.186 ppb in Baaj. Although no clinical signs and pathological changes of aflatoxicosis appeared generally, it appeared in some individual birds (Table 2).
Table 2: The results of diagnosing aflatoxicosis in the broiler chicken of 6 areas of Nineveh Province by ELISA
Areas |
Broiler farms (n) |
Broiler feed samples (n) |
titer concentration (ppb) |
Result |
permissible limit >or< from 20 ppb |
Mosul |
1 |
2 |
0.23 |
+ |
less |
2 |
2 |
||||
Hamdanya |
1 |
2 |
0.207 |
+ |
less |
2 |
2 |
||||
Talafer |
1 |
2 |
0.220 |
+ |
less |
2 |
2 |
||||
Bartella |
1 |
2 |
0.201 |
+ |
less |
2 |
2 |
||||
Baaj |
1 |
2 |
0.186 |
+ |
less |
2 |
2 |
||||
Gayara |
1 |
2 |
0.207 |
+ |
less |
2 |
2 |
Correlation between IBD and aflatoxicosis
The correlation between the IBD and aflatoxicosis in the broiler farms of the 6 areas in Nineveh Province is an incremental positive correlation but not significant in the Person correlation test (Figure 7).
Figure 7: The Pearson correlation test between IBD and aflatoxin B1 in the broiler chicken of 6 areas of Nineveh Province (October 2021-March 2022) with a significant level set on P<0.05.
Discussion
The current study investigated the prevalence of infectious bursal disease IBD and aflatoxicosis with their correlation in broilers chicken in six different areas of Nineveh Province, Iraq, namely Talafer, Hamdanya, Bartella, Baaj, and Gayara for six months (October 2021-March 2022) through diagnosis by ELISA technique. The necropsy results showed transudate or gelatinous fluid and hydropericardium in varying severity with congestion, friable, and swelling of the liver. This may be attributed to the hydropericardium hepatitis syndrome or inclusion body hepatitis caused by fowl adenoviruses or aflatoxicosis (20). In addition to the swelling, necrosis of the kidneys, and enlarged bursa of Fabricious in varying severity, which may be attributed to infected by IBD with low-rate severity (21) in addition to the few bird’s cases showed extreme paleness or fatty change of the liver which attributed to aflatoxicosis (22). These macroscopic lesions may result from simultaneous infections of these diseases, in association with other causes, or may also be attributed to other diseases and syndromes due to immunosuppression of broilers (23).
The results revealed the presence of a subclinical infection or a natural attack of the IBD virus according to the vaccine index equation attached with the measurement kit, where low titers of antibodies to the virus appeared. It is caused either by a subclinical infection or vaccination, and since most of the broiler farms in the current study areas did not have the vaccination for IBD, according to what was inquired from the owners of these farms, it was considered a subclinical infection or a natural attack of the IBD virus (24,25).
As for the results of diagnosing aflatoxin poisoning, they were positive values for aflatoxin B1 with a range of 0.186-0.23 ppb, and they are consistent with the levels of aflatoxin in broiler feed specified in the Middle East (26-28), and it did not cross the permissible rate of 20 parts per billion ppb (29). Natural contamination of chicken feeds with aflatoxicosis was recorded in many countries, such as the United States, the United Kingdom, Australia, Poland, Indonesia, Malaysia, India, Nigeria, Morocco, Sudan, and Iraq (30). Aflatoxin B1 is a toxic product for the growth of fungi, mainly produced by Aspergillus flavus and A. parasiticus in cereals, especially corn, which contains its spores and germinates during storage (22). Studies have shown that aflatoxin is immunosuppressive, and taking it with feed decreases birds' immunity. The levels of Aflatoxin B1 causing aflatoxicosis depend on the strain of the fungi and chicken susceptibility (31).
The effect of mycotoxins in poultry farming is very complex and varies significantly according to their toxicological mechanisms affecting several organs, which may lead to animal mortality in case of high contamination levels. When mycotoxins in feed combine simultaneously, they may have a synergistic or additive effect. Even when mycotoxins are low in feed during the sensitive period of the production cycle or upon prolonged exposure, they can weaken the immune system, leading to immunosuppression (32,33).
The immunosuppressive effect of aflatoxin may be related to direct inhibition of protein synthesis, including specific functions such as immunoglobulins IgG and IgA, inhibition of migration of immune cells, interference with the activity of proteolytic enzymes, reduction in the number of lymphocytes through its toxic effect on the follicle of Fabricius and impaired cytokine synthesis by lymphocytes. The rate of immunosuppression is inevitably linked to exposure to aflatoxin B1 (34,35). Our results agree with one of the studies conducted to evaluate the effects of aflatoxin-contaminated feed on the immune response of flocks of broilers to live viral attenuated bursa disease (IBD) vaccines (36). In other studies, it has been shown that aflatoxins in feed negatively affect immune responses and thus increase the susceptibility of poultry and mammals to infectious diseases. Several studies have shown that aflatoxins significantly reduce the initial immune responses and lower the IgA level, leading to IBD in poultry (37). The metabolic pathway of aflatoxin is different. Aflatoxin B1 may enter the cell and be metabolized using mono-oxygenase enzymes in the endoplasmic reticulum to hydroxylated metabolites that are also metabolized to glucuronide and conjugated sulfate, or it may be oxidized to a functional epoxide that undergoes spontaneous hydrolysis to aflatoxin B1-8,9-dehydrodihydrofol. It binds with proteins, causing cytotoxicity. The epoxide release can be reacted with DNA or protein or detoxed by inducing glutathione sulfide transporters to convert to conjugated glutathione (38).
One study showed that exposure of chickens to subclinical levels of aflatoxin in feed leads to some effects on the immune system. This can be especially dangerous when the exposure is concurrent with exposure to an infectious virus such as lymphotropic, and during field infection in chickens, it can cause severe lesions of the Fabricius follicle (39). The reason for the emergence of the weak relationship between contamination with aflatoxin and IBD may explain the fact that the season of collecting samples was in periods of low temperatures, the reasons for the increased production of mycotoxins, especially aflatoxins, or because of the relatively good biosecurity and the broiler feed storage conditions for poultry farms in our study (40). This study indicated a positive correlation between IBD and aflatoxicosis but was insignificant. It appears that bird immunity has essential roles in such cases, that aflatoxin is one of the immunosuppressants, and the use of more cost-effective solutions to prevent aflatoxin from reaching the food chain contributed reduce its harmful effects.
Conclusion
The detection of both IBD and aflatoxicosis occurred by the ELISA technique. The necropsy results showed hydropericardium, paleness or congestion, friable and swelling of the liver, kidneys, and bursa of Fabricius, with more severe lesions in a few sporadic cases as gelatinous fluid surrounding the heart, intense paleness of the liver, kidney, and enlarged bursa of Fabricius. The detection of IBD by ELISA revealed that the positive results were 142, and the negative results are 8 birds out of a total of 150 suspected broiler attributed to the subclinical infection according to the vaccine index equation. Also, positive aflatoxin B1 concentrations by ELISA were recorded in all broiler feed in the 6 areas as the highest concentration mean was 0.23 ppb and the lowest concentration mean was 0.186 ppb in Mosul and Baaj, respectively. This study indicated a positive correlation between IBD and aflatoxin B1 but was not statistically significant.
Acknowledgments
We would like to thank the College of Veterinary Medicine, University of Mosul for supporting this work.
Conflict of Interest
There is not any conflict of interest.
1- This study aimed to investigate the incidence of infectious bursal disease IBD and aflatoxicosis with their correlation.
2- Positive detection of IBD as 94.6% of total 150 tested serum, attributed to the subclinical infection.
3- The highest aflatoxin B1 concentration mean was 0.23 ppb in Mosul and the lowest was 0.186 ppb in Baaj.
4- This study indicated a positive correlation between IBD and aflatoxin B1 but was not statistically significant.
- Dey S, Pathak DC, Ramamurthy N, Maity HK, Chellappa MM. Infectious bursal disease virus in chickens: Prevalence, impact, and management strategies. Vet Med. 2019;10:85-97. DOI: 10.2147/VMRR.S185159
- Mwenda RK, Changula BM, Hang N, Chidumayo AS, Mangani T, Kaira A, Takada AS, Mweene E. Characterization of field infectious bursal diseaseviruses in Zambia: Evidence of co-circulation ofmultiple genotypes with predominance of very virulent strains. Avian Pathol. 2018;47:300-313. DOI: 10.1080/03079457.2018.1449941
- Fanar A Isihak, Hana Kh Ismail, Abdulwahid A Wahid. Comparison study between the efficacy of immune complex and conventionally live vaccine against Gumboro disease in broilers. Iraqi J Vet Sci. 2021;35, 4, 627-632. DOI: 10.33899/ijvs.2020.127366.1499
- Muller H, Islam M, Raue R. Research on infectious bursal disease the past, the present and the future. Vet Microbiol. 2003;97:153-165. DOI: 10.1016/j.vetmic.2003.08.005
- Parker D, Wit S, Houghton H, Prandini F. Assessment of impact of a novel infectious bursal disease (IBD) vaccination program in breeders on IBD humoral antibody levels through the laying period. Vet Rec Open. 2013;1(1):1-2. DOI: 10.1136/vropen-2013-000016
- Swayne DE. Diseases of Poultry. NY: Wiley; 2013.
- Wagari A. A review on infectious bursal disease in poultry. Hlth Econ Outcome Res. 2021;7(2):018-023. DOI: 10.4172/2471-268x
- Fouad AM, Ruan D, El-Senousey HK, Chen W, Jiang S, Zheng C. Harmful effects and control strategies of aflatoxin b₁ produced by Aspergillus flavus and Aspergillus parasiticus strains on poultry: Review. Toxins. 2019;11(3):176. DOI: 10.3390/toxins11030176
- Saud Basher H, Mushtaq T AL-Zuhariy. Using T cell lymphokines to enhance the immune response against Newcastle disease in vaccinated broiler chickens fed naturally contaminated diet with different mycotoxins. Iraqi J Vet Sci. 2020;34(2):427-433. DOI: 10.33899/ijvs.2019.125977.1204
- Shao Y, Duan H, Zhou S, Ma T, Guo L, Huang X, Xiong Y. Biotin-streptavidin system-mediated ratiometric multiplex immunochromatographic assay for simultaneous and accurate quantification of three mycotoxins. J Agric Food Chem. 2019;67(32):9022-9031. DOI: 10.1021/acs.jafc.9b03222
- Huang X, Liu Y, Yung B, Xiong Y, Chen X. Nanotechnology-enhanced no-wash biosensors for in vitro diagnostics of cancer. ACS Nano Soci. 2017;11(6):5238-92. DOI: 10.1021/acsnano.7b02618
- Yunus AW, Razzazi E, Bohm J. Aflatoxin B1 in affecting broiler's performance, immunity, and gastrointestinal tract: A review of history and contemporary issues. Toxins. 2011;3(6):566-90. DOI: 10.3390%2Ftoxins3060566
- Dong X, Zou B, Zhao X, Liu S, Xu W, Huang T, Wang S. Rapid qualitative and quantitative analysis of aflatoxin B1 in Pu-erh tea by liquid chromatography- isotope dilution tandem mass spectrometry coupled with the QuEChERS purification method. Anal Methods. 2018;10(39):4776-4783. DOI: 10.1039/c8ay01730a
- Ahmed ME, Ravikanth K, Rekhe DS, and Maini S. Histopathological alterations in Aflatoxicity and its amelioration with herbomineral toxin binder in broilers. Vet World. 2009;2(10):390-392. [available at]
- Mahajan, A, Katoch RC, Chahota R, Verma S, and Manuja, S. Concurrent outbreak of infectious bursal disease (IBD), aflatoxicosis and secondary microbial infection in broiler chicks. Vet Arh. 2002;72(2):81-90. [available at]
- Murugesan GR, Ledoux DR, Naehrer K, Berthiller F, Applegate TJ, Grenier B, Phillips TD, Schatzmayr G. Prevalence and effects of mycotoxins on poultry health and performance, and recent development in mycotoxin counteracting strategies. Poult Sci. 2015;94(6):1298-315. DOI: 10.3382/ps/pev075
- Maxwell OO, Mukiibi-Muka G, Bisgaard MC. Aflatoxicosis, infectious bursal disease and immune response to Newcastle disease vaccination in rural chickens. Avian Path. 2005;34:319-323. DOI: 10.1080/03079450500179327
- Jarjees MT, Jwher DM. Studying an outbreak of inclusion body hepatitis in broilers in Nineveh governorate, Iraq. Iraqi J Vet Sci. 2022;36(3):769-74. DOI: 10.33899/ijvs.2022.131932.2024
- Hameed HM, Maty HN, Hassan AA. Effect of dietary BHA supplementation on certain physiological values in broiler chicken. Iraqi J Vet Sci. 2022;36(3):815-9. DOI: 10.33899/ijvs.2022.132202.2068
- Chen Z, Shi S, Qi B, Lin S, Chen C, Zhu C, Huang Y. Hydropericardium syndrome caused by fowl adenovirus serotype 4 in replacement pullets. J Vet Med Sci. 2019;81(2):245-251. DOI: 10.1292/jvms.18-0168
- Omer MG, Khalafalla AI. Epidemiology and laboratory diagnosis of very virulent infectious bursal disease virus in vaccinated chickens in Khartoum, Sudan. Open Vet J. 2022;12(1):33. DOI: 10.5455/OVJ.2022.v12.i1.5
- Samuel N, Ezri Y, Farah R, Igor V, Hussein A, Rubinshtein O, Assy N. Acute aflatoxicosis resulting in fulminant hepatic failure and rhabdomyolysis. Gastroenterol Res. 2009;2(1):48-50. DOI: 10.4021/gr2009.01.1254
- Schat KA, Skinner MA. Avian immunosuppressive diseases and immunoevasion. Avian Immun. 2014;275-97. DOI: 10.1016/B978-0-12-396965-1.00016-9
- Liu D. Infectious Bursal Disease Virus. NY: CRC Press; 2016. 629-36 p.
- Kabell S, Handberg KJ, Li Y, Kusk M, Bisgaard M. 2005. Detection of vvIBDV in Vaccinated SPF Chickens. Acta Vet Scand. 2005;46:219-227. DOI: 10.1186/1751-0147- 46-219
- Naveed M, Haleem KS, Ghazanfar S, Tauseef I, Bano N, Adetunji CO, and Paray BA. Quantitative estimation of aflatoxin level in poultry feed in selected poultry farms. Biol Med Res Int. 2022;5397561:1-7. DOI: 10.1155/2022/5397561
- Korley Kortei N, Akomeah Agyekum A, Akuamoa F, Baffour VK, Wiisibie H. Risk assessment and exposure to levels of naturally occurring aflatoxins in some packaged cereals and cereal-based foods consumed in Accra, Ghana. Toxicol Rep. 2018;6:34-41. DOI: 10.1016/j.toxrep.2018.11.012
- Kehinde HW, Sekoni AA, Olugbemi TS, Onimisi PA. Prevalence of aflatoxin b1 in some common poultry feed ingredients and optimum inclusion levels of mycofix binder as feed additive on performance of broiler chickens. Nigerian J Anim Prod. 2018;45(2):137-49. DOI: 10.51791/njap.v45i2.495
- Sarma UP, Bhetaria PJ, Devi P. et al. Aflatoxins: Implications on Health. Indian J Clin Biochem. 2017;32:124-133. 10.1007/s12291-017-0649-2
- Ditta YA, Mahad S, Bacha U. Aflatoxins: Their toxic effect on poultry and recent advances in their treatment. London: Intech Open; 2022. 23-90 p.
- Dhanasekaran D, Shanmugapriya S, Thajuddin N, Panneerselvam A. Aflatoxins and Aflatoxicosis in Human and Animals. Biochem Molecul Biol. 2011;34:90-99. DOI: 10.5772/22717
- Bennett JW, Klich M. Mycotoxins. Clin Microbiol Rev. 2003;16(3):497-516. DOI: 10.1128/CMR.16.3.497-516.2003
- Etrradossi N, Saif YM. Infectious bursal disease. USA: Wiely; 2020. 257-283 p.
- Benkerroum N. Chronic and acute toxicities of aflatoxins: Mechanisms of action. Int J Environ Res Public Hlth. 2020;8;17(2):423. DOI: 10.3390/ijerph17020423
- Naseem MN, Saleemi MK, Khan A, Khatoon A, Gul ST, Rizvi F, Fayyaz A. Pathological effects of concurrent administration of aflatoxin B1 and fowl adenovirus-4 in broiler chicks. Microbial Pathog. 2018;121:147-154. DOI: 10.1016/j.micpath.2018.05.021
- Gabal MA, Azzam AH. Interaction of aflatoxin in the feed and immunization against selected infectious diseases in poultry. II. Effect on one‐day‐old layer chicks simultaneously vaccinated against Newcastle disease, infectious bronchitis, and infectious bursal disease. Avian Path. 1998;27:290-295. DOI: 10.1080/03079459808419338
- Azzam AH, Gabal MA. Interaction of aflatoxin in the feed and immunization against selected infectious diseases. Avi Pathol. 1997;26:317-325. DOI: 10.1080/03079459708419214
- Marchese S, Polo A, Ariano A, Velotto S, Costantini S, Severino L. Aflatoxin B1 and M1: Biological properties and their involvement in cancer development. Toxins (Basel). 2018;10(6):214. DOI: 10.3390/toxins10060214
- Pierron A, Alassane I, Oswald IP. Impact of mycotoxin on immune response and consequences for pig health. Anim Nutr. 2016;2(2):63-8. 10.1016/j.aninu.2016.03.001
- Ren M, Xu H, Huang X, Kuang M, Xiong Y, Xu H, and Wang A. Immunochromatographic assay for ultrasensitive detection of aflatoxin B1 in maize by highly luminescent quantum dot beads. ACS Appl Mater Interfaces. 2014;6(16):14215-14222. DOI: 10.1021/am503517s
- Article View: 173
- PDF Download: 106