Mineralogically Well
Characterized Bentonite Sources Controlled Aflatoxin Contamination in Poultry
Ahmad Khan1*, Mohammad Saleem Akhtar1,
Saba Akbar1, Khalid
Saifullah Khan1, Tanveer Ahmad2 and Nasir Mukhtar3
1Institute of Soil Science, PMAS Arid Agriculture
University Rawalpindi, Pakistan
2Department of Livestock Production & Management,
PMAS Arid Agriculture University Rawalpindi, Pakistan
3Department of
Poultry Science, PMAS Arid Agriculture University Rawalpindi, Pakistan
*For correspondence: ahmadk78@gmail.com
Received 24 April 2021; Accepted 17 June 2021; Published
30 March 2022
Abstract
Aflatoxin in
poultry feed reduces production, and is a health hazard to the consumers. Its
toxicity is reduced through addition of clays. Evaluation of the country’s
bentonites may promote their use as toxin binder. After detailed
mineralogical and aflatoxin adsorption characteristics of large number of
indigenous quarries effectiveness of two bentonites was determined through
feeding trial. Bentonites from Bhimber and Dina quarries were applied in
three replications
at 1 and 2% (w/w) with positive and negative controls to a feed
containing 250 µg kg-1 aflatoxin B1. Ten birds initially fed
on clean starter feed for two weeks, fed on the experimental feeds and
slaughtered after recording live weight on day 35 and dress weight along with
internal organs weight were recorded with any apparent disorders. While addition
of the bentonites had no detrimental effect, aflatoxin contamination had the
lowest body weight and weight gain rate, reduced feed intake and feed
conversion ratio with apparent disordered liver. The live body weight and
weight gain rate increased with 2% bentonite addition to the contaminated feed
from both the sources and was statistically similar to the clean feed though
the values for these parameters were highest when the addition was to the clean
feed. A 42% reduction occurred in weight gain without smectite addition in the
toxin feed. The toxin feed had the lowest absolute liver and heart weight with
dark coloration. The bentonites use in feed industry may reduce aflatoxin
incidences at the application rate of 2%. © 2021 Friends Science Publishers
Keywords: Bentonite; Aflatoxin; Poultry; Contaminated feed; Adsorption;
Growth performance
Introduction
Aflatoxins
are carcinogenic mycotoxins (IARC 2002)
that occur in poultry feed, reduce production and pose health risk to the
consumers (Sana et al. 2019). The
critical limit of aflatoxin in feed is 20 µg kg-1 (Stoloff et
al. 1991). The incidence rate of feed contamination as high as 83% has been
reported in Pakistan (Khan et al. 2013;
Iqbal et al. 2014) and the level of contamination increases
during rainy months (Anjum et al. 2012).
Aflatoxin contamination beyond the regulatory level may induce economic losses (Kana et al. 2010) through
immune-suppression, poor growth with high feed intake and low efficiency for
feed conversion (Naseem et al. 2018; Al-Ruwaili
et al. 2018).
Smectite containing geologically occurring clays are called bentonites
and their addition in the contaminated animal and poultry feed is an effective
control measure (Pasha et al. 2007). Adsorption of aflatoxin from the gastro-intestinal tract occurs in the
interlayer of smectite through ion-dipole interaction and H-bonding (Deng et al.
2010). The amendment rate and mineralogical
characteristics of the clays have been reviewed (Huwing
et al. 2001; Dixon et al. 2008). The mineral purity and
mineralogical properties that leads to fast kinetics of adsorption with high
binding strength and no dissociation in the gastrointestinal tract are
important features for considering for use as a feed additive (Li et al. 2010). Several bentonite
based binders including Novasil plus, Astra
ben 20A and hydrated sodium and calcium aluminosilicates (HSCAS) are
commercially available (Bailey et al. 2006) while Mycofix, the first bentonite based binder recommended by
European Commission, possess > 90% adsorption efficiency (European Commission 2013). The bentonite with dominance of calcium on exchange sites is more effective as aflatoxin adsorbent than
those with sodium (McClure et al. 2014).
Bentonite improves serum enzymatic activity in an incidence of severe
aflatoxicosis in broiler birds (Bhatti et al. 2016).
Smectite
application at the rate of 0.25 to 2% effectively reduce aflatoxin toxicity in
poultry and animals (Phillips et al.
2008; Kermanshahi et al. 2009). Addition of calcium bentonite reduces
accumulation of aflatoxin B1 residues in liver (Fowler
Table 1: Experimental poultry feed composition
Feed
ingredients |
Application
Rate (kg 100 kg-1) |
Corn |
45 |
Soybean
meal |
17 |
Soybean
grain |
5 |
Wheat |
5 |
Canola meal |
6 |
Rice polish |
5 |
Wheat bran |
5 |
Di-calcium
phosphate |
1 |
Premix |
1 |
Corn gluten
30% |
4 |
Corn gluten
60% |
2 |
Molasses |
3 |
Table 2: Poultry feeding trial details
Treatments |
Treatment
ID |
Clean feed
+ no clay no toxin |
CF |
Toxin feed
+ no clay |
TF |
Clean feed
+ Bhimber bentonite @ 2% |
CFB-I |
Clean feed
+ Dina bentonite @ 2% |
CFB-II |
Toxin feed
+ Bhimber bentonite @ 1% |
TFB-I-1 |
Toxin feed
+ Bhimber bentonite @ 2% |
TFB-I-2 |
Toxin feed
+ Dina bentonite @ 1% |
TFB-II-1 |
Toxin feed
+ Dina bentonite @ 2% |
TFB-II-2 |
et al. 2015) and improves
humoral immunity against Newcastle Disease (Wafaa
et al. 2013). Smectite is a superior feed additive than palygorskite and zeolite (Dixon
et al. 2008).
Due to complex gut conditions the feeding experimental data may differ with
the in vitro aqueous adsorption calculated from the batch studies and fitting (Kannewischer et al. 2006). A large mismatch with estimated adsorption and an
effective control determined through feeding trials have been reported (Barrientos-Velazquez and Deng 2020). Aflatoxin adsorption studies using natural or synthetic
gastric fluids are limited (Li et al.
2010).
Systematic feeding experiments on the bentonites with their complete
mineral characterization have limited the use of indigenous sources as a
potential aflatoxin adsorbent. The study evaluates the efficacy of indigenous
bentonite selected after detailed characterization from a large number of
quarries from the country. While detailed mineralogical characteristics and
adsorption potential are available, the study evaluates two application rates
on weight gain, feed consumption and disorders in internal organs for the two bentonites.
Materials and Methods
Experimental
details
The bentonite
sources: (i) Bhimber, AJK and (ii) Dina, Punjab were
selected for the feeding experiment for which the relevant mineralogical and aflatoxin
adsorption characteristics were known. Two feed stocks were prepared: (i) clean feed having aflatoxin contamination < 20 µg
kg-1 and (ii) contaminated feed with 250 µg kg-1
aflatoxin B1 in the final preparation. The feed ingredients were tested for
their total and aflatoxin B1 levels using an Enzyme-linked immuno-sorbent assay
(Barabolak 1977) and for the feed stock ii, naturally
contaminated wheat, maize and soyabean meal were mixed proportionately (Table
1) for the final aflatoxin B1 contamination level of 250 µg kg-1.
The bentonite amendments (Table 2) were homogenized by using a feed mixer for
15 min, and remained stored under controlled humidity and temperature
conditions.
One day old broiler chicks from a commercial hatchery
were reared on the clean feed for the first two week maintaining shed
temperature of 32°C and relative humidity of 70%. The shed temperature was
reduced 3°C per week until 22°C and was maintained thereafter. Birds were
provided with ad libitum access to feed and water throughout the experiment. At
day 14, the birds were distributed in the designated treatments with 10 birds
per pen in a way that each replicated pen had similar average weight. The birds
were fed on the experimental feeds during the following three weeks. The
vaccination schedule as recommended by the National Disease Control Committee
in Pakistan was followed. Daily health and mortality, weekly body weight gains
were recorded during the experimental period. The feed offered, feed retained
and body weight per pen were recorded at day 21, 28 and 35. Live weight of
randomly selected three birds from each replicated pen was recorded on day 35
and slaughtered. The dress weight and the weight of liver, heart and spleen
were recorded. Apparent deformation of internal
Fig 1: Mineral
composition of indigenous bentonite sources having dominant smectite (Sm) with traces of quartz (Q), calcite (C) and mica (M) as
identified by X-ray diffraction analysis
Fig 2: Live body
weight over the feeding weeks indicating the clays addition to the contaminated
feed at 2 % reduced toxic effect
organs was also examined.
The temporal
data for body weight, weight gain, feed consumption and feed conversion ratio
were subjected to a multivariate analysis using SAS/STAT® version 9.4. (SAS
Institute Inc. 2002) repeated for the weeks. Variation in the absolute and
relative weight of the internal organs and dressing percentage was analyzed by
an ANOVA under Completely Randomized Design (CRD). Treatment means were
compared using Tukey’s HSD test at p < 0.05.
Results
Both
the bentonites from Bhimber and Dina had relatively pure smectite while illite, kaolinite and quartz occurred as traces in Bhimber,
and Dina had same component minerals with calcite in moderate amount (Fig. 1).
Smectite was identified as dioctahedral montmorillonite with aluminium dominance
at octahedral positions. Bhimber had isomorphic substitution of Mg in octahedra
while Dina had Fe2+/Fe3+ for Al. The maximum aflatoxin
adsorption capacity (Qmax) of Bhimber was
500 µg
g-1 while
for Dina it was 750 µg
g-1 of clay. The bentonites amendments to the
feed reduced aflatoxin toxic effect as seen through an improved body weight,
feed intake and weights of internal organs. The clays as had no negative impact
on the broiler health, and caused gain in body weight when added to the clean
feed. The results are presented in detail as follows.
Body weight
Live weight
in a particular pen recorded on weekly basis divided with the number of living
birds in each pen was an average body weight per bird (Fig. 2). The body weight
varied with the treatment differently over the experimental feeding weeks as
the hypothesis of no week × treatment effect was rejected (MANOVA test
criteria Wilks’ Lambda p ≥ 0.0001).
At week 1 on
experimental diets, (day 21) the body weight changed significantly (p <
0.0001) and was the highest, 898 g bird-1, with the clean feed
followed by the clean feed with the bentonite from both sources. The toxin
containing feed had the lowest body weight, 731 g bird-1 that was
similar to the toxin feed with 1% of the two bentonite sources. At day 28, the
body weight in the clean feed was at par with the toxin feed with bentonites
addition from both the sources at 1 and 2%. The toxin feed had the lowest body
weight, 959 g bird-1, that was significantly different with all the
other treatment combinations (p = 0.0073). At day 35, the highest body weight
of 1765 g bird-1 was with the clean feed with Bhimber bentonite and
was significantly different than all other treatment combinations. Both
bentonite sources at 1% were at par and only higher to the toxin feed that had
the lowest body weight of broilers, 1127 g bird-1. The clean feed
had similar body weight as in the toxin feed with 2% application of both
bentonites. Overall, the toxic
effect of aflatoxin contamination was reduced by the bentonite sources at 2% and the clays addition in the clean feed
had no negative impact on broilers body weight.
Weight gain
rate
Body weight
gain in broilers during the three weeks of experimental feedings had
significant variation (p < 0.0001) due to the treatment combinations (Fig. 3).
The aflatoxin containing feed had 42% lower body weight gain than with the bentonite addition at 2% from any
of the two clays. The clean feed with bentonite from Bhimber was significantly
different than all the other combinations, and had the highest weight gain
(1300 g bird-1). The birds fed on the contaminated feed gained only
661 g bird-1 during the experimental period resulting in a reduced
production. At 1% application rate both bentonite sources in toxin feed were
only better in weight gain than contaminated feed suggesting 1% was as a low application
level. Both the bentonites at 2% application and the clean feed had similar
weight gain.
Weight gain
over the experimental feeding weeks changed significantly. After first week the
higher body weight gain recorded in the clean feed whether or not the clay was
added which differed significantly from the toxin feed. Aflatoxin contamination
reduced weight gain to only 228 g bird-1 during second week and 168
g bird-1 during third week. During third week 2% clays addition in
contaminated feed gained lower weights than in second week. Overall, both the
bentonite sources improved growth and weight gain in birds in the clean as well
as the toxin containing feed.
Feed intake
The average
feed consumed in each pen was recorded weekly after subtracting the amount of
feed retained from the feed offered, and the feed consumed divided with the
number of living birds in a particular pen was an average feed consumed per
bird (Fig. 4). The hypothesis of no week × treatment effect was rejected
through the test statistics Wilks' Lambda from the MANOVA (p = 0.006). Feed
consumption varied significantly (p = 0.0002) with treatments at different
weeks and was also significantly correlated.
While the feed
intake at day 21 was non-significant, feed consumption in week 2 on
experimental diets (28 day) varied significantly with the treatment
combinations (p < 0.0001). The toxin feed with Bhimber bentonite at 2% rate
of application had the highest feed intake that was similar to the clean feed
with the same bentonite. The lowest feed intake was observed in the toxin feed
and was at par with clean feed with Dina bentonite. The treatment means also
varied significantly for feed intake on week 3 (p < 0.0001). The clean feed
with Dina bentonite had the highest feed consumption that was similar to the
clean feed and the clean feed with Bhimber bentonite. The toxin feed with both
bentonite sources at 1 and 2% were statistically at par. The lowest feed intake
was recorded in the toxin feed that differed significantly with all the other
treatment combinations.
Fig 3: Body weight gain over three experimental weeks
indicating the lowest weight gain on the toxin feed and increase under the bentonite
addition to the contaminated feed
Fig 4: Weekly feed consumption representing the lowest feed
intake with the toxin feed whereas the clean feed with and without bentonite
had the highest feed consumption
Feed
conversion ratio
The
efficiency of broilers in converting consumed feed to body weight was
demonstrated by their feed conversion ratio (Fig. 5). Feed conversion ratio
varied significantly (p < 0.0001) with treatment combinations at different
weeks. After first week on experimental feeds, day 21, the treatment
combinations differed significantly for the feed conversion ratio (p <
0.0001). The highest feed conversion ratio, 2.4, was determined in the toxin
feed that significantly varied with all the other feed combinations. Both the
bentonite sources at 1 and 2% in the toxin containing feed were similar. The
clean feed with Dina bentonite had the lowest feed conversion ratio and was at
par with the clean feed along with the clean feed with Bhimber bentonite
suggesting better conversion of feed to body mass. The feed conversion ratios
generally increased on second week of experimental feedings irrespective of
feed combinations. At 28 day the highest feed conversion ratio was associated
with the toxin feed that was similar to the toxin feed with Bhimber bentonite
at both levels (1 and 2%) and the clean feed with both bentonite sources. At
the final week, day 35, the toxin feed had the highest feed conversion ratio,
3.49, that varied significantly with all the other treatment combinations. The
lowest feed conversion ratio was in the toxin feed with Bhimber bentonite and
was at par with all other treatments except the toxin feed. Overall, the toxin
containing feed had higher feed conversion ratio at each week and the clay
sources addition in both the clean feed and the toxin feed demonstrated lower
feed conversion ratio suggesting improved feed conversion efficiency in the
experimental birds.
Dressing
percentage
The treatment
effect on the dressing percentage was significant (F 9.53, df 7; p < 0.0001)
(Fig. 6). The toxin feed with Dina bentonite at 2% yielded the highest dressing
percentage, 65.9%, followed by the clean feed with any of the two bentonites.
The dressing percentage for all other feed combinations was non-significant
except the toxin feed. The toxin feed had the lowest dressing percentage, 57.3%
which was significantly lower than all the other treatment combinations.
Internal
organs weight
Absolute and
relative weights of liver, heart and spleen (Table 3) were compared. The
treatment combinations had significant effect on absolute liver (F 5.69, df 7;
p < 0.0019) and heart weights (F 2.94 df 7; p < 0.0351). The highest
liver weight was in the clean feed with Bhimber bentonite. It had lesions that
was similar to that of in the toxin feed with Dina bentonite at 2% and the
toxin feed with bentonite from Bhimber at 1%. The highest heart weight, 13.6 g,
was in the toxin feed with 1% Bhimber bentonite which was at par with the toxin
feed with 2% bentonite from Dina and the clean feed. The lowest liver, 30.9 g,
and heart weight, 9.4 g, were observed in the toxin feed. The toxin containing
feed with Bhimber bentonite at 1% had liver morphology similar to the clean
feed. The spleen in terms of its absolute and relative weight was
non-significant. Therefore, Table 3: Absolute and relative weight of internal
organs
|
Absolute
weight (g) |
Relative
weight (%) |
|||||
Treatments |
Liver |
Heart |
Spleen |
Liver |
Heart |
Spleen |
|
|
……………………….….
grams ……………………… |
………………………..
% ………………………… |
|
||||
CF |
42.63 7.61 b |
11.62 0.88 ab |
2.09 0.30 a |
2.30 0.42 b |
0.63 0.04 bc |
0.11 0.01 a |
|
TF |
30.90 3.28 c |
9.40 0.72 c |
1.690.38 a |
2.28 0.15 b |
0.70 0.07 ab |
0.12 0.03 a |
|
CFB-I |
54.250.77 a |
11.33 0.75 bc |
2.49 0.38 a |
2.83 0.10 a |
0.59 0.02 c |
0.13 0.02 a |
|
CFB-II |
43.32 5.65 b |
11.53 1.97 b |
2.23 0.24 a |
2.32 0.10 b |
0.62 0.07 bc |
0.12 0.01 a |
|
TFB-I-1 |
46.09 2.39 ab |
13.68 1.65 a |
2.53 0.71 a |
2.47 0.07 ab |
0.73 0.05 a |
0.14 0.04 a |
|
TFB-I-2 |
41.78 7.65 b |
11.02 0.37 bc |
2.62 1.05 a |
2.39 0.40 b |
0.63 0.01 bc |
0.15 0.06 a |
|
TFB-II-1 |
41.39 0.75 b |
10.92 1.09 bc |
2.12 0.13 a |
2.44 0.13 ab |
0.64 0.02 abc |
0.12 0.01 a |
|
TFB-II-2 |
47.34 4.09 ab |
11.76 1.25 ab |
1.88 0.48 a |
2.58 0.15 ab |
0.64 0.06 abc |
0.10 0.02 a |
|
Values (Mean ± SD)
in each row followed by different
letters are significantly different (p ≤ 0.05). For analysis, 3 birds
were selected randomly from each replicate of treatment combinations at day 35
and the data collected were analyzed by applying ANOVA
Fig 5: Weekly feed conversion ratio indicating detrimental
effect of the toxin feeding while the lower FCR was with the clay’s addition in
both the clean feed and the toxin feed
Fig 6: Dressing percentage with the lowest values in the toxin
feed that improved with the clay’s addition at both applied levels from the two
sources in the clean and the toxin feed
among the
internal organs absolute liver and heart weight varied while the relative
weight of all the three internal organs (liver, heart and spleen) did not
change suggesting equal effect of toxin feeding on the internal organs weight.
Discussion
The lowest
body weight at each experimental week in the toxin containing feed explained
the toxic effect of contaminated feedings. Aflatoxin toxicity affects the body weight gain, feed intake
and broilers health suggesting interference of aflatoxin in the digestive
system (Hassan et al. 2012) and results in reduced poultry
production (Pasha et al. 2007; Naseem
et al. 2018). The toxin feed
reduce synthesis of protein and lipids loss with droppings, reduction in
nutrients assimilation and less production of digestive glands (Verma et al.
2002). Aflatoxin effect started from the first week
on experimental feeds resulting in the lowest body weight in the toxin
containing feed. Therefore, the kinetics of aflatoxin effect on body weight is
fast though the repeat effect occurred from the second feeding. Broilers growth
and production is reduced by aflatoxin contamination above critical level (Kana et al. 2010). Body weight and
body weight gain is also affected by toxin level and exposure time (Heba and Hesham 2004; Mahmood et al. 2017). Feeding aflatoxin results in higher feed conversion ratio
with lower body weight gain, and is generally agreed (Pasha et al.
2007).
Reduction in the weight gain may be related to the inability of the birds fed
on the toxin feed to consume and digest dry ration and amino acids.
Contaminated diet results in high feed conversion ratio during experimental
period and is related to reduced efficiency of broilers. Our findings were
consistent with the toxic effects of feeding aflatoxin contaminated feed in
broilers (Shi et
al. 2006).
A low weight gain at each experimental week suggest progressive
reduction and is related to dose and prolonged exposure to aflatoxin feeding (Mahmood et al. 2017). Inconsistent weight gain reduction
has also been reported mainly due to the duration and level of the aflatoxin
exposure. The toxin results in stunted and ruffled chickens with a reduction in
weight gain (Bhatti et al. 2018; Naseem et al. 2018). Aflatoxin
feeding also reduce feed consumption and efficiency of feed conversion (Mahmood
et
al. 2017) and is in agreement with the previous
studies (Heba and Hesham 2004; Pasha et al.
2007).
A variability
occurs between the adsorption capacity measured in a laboratory and the feeding
trial results (Jaynes et al. 2007)
and indicates the effectiveness of mycotoxin binders in real gut conditions.
The clays addition up to 2% in the clean feed results in better weight gain and
health with improved feed conversion ratio suggesting positive impact of clays
even at low or no aflatoxin contamination. The improvement of body weight in
the clean feed with clays addition may be associated with adsorption of any
harmful bacteria or mycotoxin other than aflatoxin present in the clean feed (Xia et al. 2004). Increase in body
weight by the clays addition in the clean feed with no and/or low contamination
levels occur (Pappas et al. 2014).
Contradictory results for improved weight gain with bentonites addition in the
clean feed relates to the non-selective adsorption of smectite (Bailey et al. 2006). Our findings
suggest safe use of both the bentonite sources at 1 and 2% with no negative
impact on weight gain and feed consumption.
Quality smectites
have been found effective in reducing the
toxicity of aflatoxin in the feed. Bentonites with high adsorption in the
laboratory estimation reduces the toxin effect (Boudergue
et al. 2009). The toxic effect of aflatoxin in broilers is
reduced by adding bentonites (Wafaa et al.
2013). Bentonite addition in the contaminated feed is not limited to aflatoxin adsorption and is also reported to boost
enzymatic activities in the gastro-intestinal tract of the birds (Xia et al. 2004). Complete recovery
from the toxic effects of aflatoxin contamination can occur by 5% application
of hydrated sodium calcium aluminosilicate (Sehu
et al. 2007). Bentonites addition at 2% ameliorated the negative
effect of aflatoxin. Addition of clay binders at concentration higher than 5%
may result in nutritional deficiency and lower production in birds (Mabbett 2005).
Lower body
weight, high mortality, poor feed conversion ratio, immunosuppression and
clinical disorders are related to aflatoxin feeding (Naseem et al. 2018;
Bhatti et al. 2018; Saleemi et al.
2020). A
reduction in the feed intake occur in response to the contaminated diets in
broilers (Rauber et
al. 2007), with liver
lesions as basic symptoms of aflatoxin toxicity (Johri
and Majumdar 1990). Aflatoxin fed broilers demonstrate gross and
histopathological lesions on the liver, kidney and bursa of Fabricius
(Ortatatli and Oguz 2001).
The experimental feed combinations affect the absolute liver and heart weight
with higher weight in the contaminated feed with 1% bentonite from Bhimber and
2% Dina bentonite. Aflatoxin feed results in the lower absolute weight of liver
and heart. However, in most studies enlarged liver and kidney
have been reported due to aflatoxin feedings (Miazzo
et al. 2005; Wafaa et al. 2013). Internal organs
especially liver respond to aflatoxin feedings with deformation in morphology
and absolute weight. In our study darkish liver with small size in the toxin
fed birds may be attributed to severe immune suppression (Kubena et al. 1990). In contradiction,
enlarged liver have been reported in the toxin fed birds over the clean feed (Tessari et al. 2006). In addition to liver
the internal organs including kidney, heart and spleen may be affected by
feeding contaminated feed to broilers (Quezada et
al. 2000). However, non-significant difference for spleen weight
among the treatments with greater variability among the replicates suggest
inconsistent response of internal organs towards toxin feedings which may be
due to lower level of aflatoxin contamination compared to other studies where
high aflatoxin doses have been tested. Non-significant variation in the
relative weight of internal organs may be associated with the low application
levels of clays as the internal organs weight is non sensitive at clay level
below 5% (Barrientos-Velazquez and Deng 2020).
Conclusion
The feeding
experiment suggested both bentonite sources were effective in reducing the
toxic effect of aflatoxin. Addition of both bentonites had no negative impact
on broilers growth and production suggesting safe use of these clays as toxin
binder. Smectite addition in the feed containing 250 µg aflatoxin kg-1
had similar body weight, internal organs morphology, and feed conversion ratio
as that of clean feed where without smectite 42% body weight reduction had
occurred. Use of indigenous smectite clays as aflatoxin binder appears to have
great potential that can reduce import of binders and control aflatoxicosis in
poultry industry of Pakistan.
Acknowledgements
The first author acknowledges Higher Education Commission of Pakistan for
PhD Fellowship of which this is part experiment. The authors would also like to
acknowledge the Department of Poultry Science, PMAS Arid Agriculture University
Rawalpindi, Pakistan for providing experimental shed and technical guidance.
Author
Contributions
MSA, TA and AK
planned the experiment, AK and SA carried out the trial and interpreted the
results, MSA and KSK guided during writeup, NM and TA supervised and guided
during the trial, MSA helped during statistical analysis, and AK made
illustrations and completed writeup
Conflicts of Interest
The authors
declare no conflict of interest.
Date
Availability
The data will be available on a fair request.
Ethics
Approval
All the ethical policies regarding animal health approved from the
University Ethics Committee were adhered and the research meet the standards
for the protection and use of animals for scientific purposes.
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