Received: 04/09/2024 Accepted: 06/11/2024 Published: 14/01/2025 1 of 7
https://doi.org/10.52973/rcfcv-e35512 Revista Cientíca, FCV-LUZ / Vol. XXXV
ABSTRACT
Essential oils have demonstrated beneficial effects on the
productive parameters of poultry. However, the impact of
nanoencapsulated essential oil blends (N–EOs) in the diet of laying
hens has been little described. The objective of the research was to
evaluate the effect of mixtures of N–EOs in diets of Lohmann Brown
hens on the percentage of laying, quality, and oxidative stability
of the egg product. 600 birds were randomly distributed into ve
groups (n=150 per group), according to a completely randomized
design, receiving the control group (T0) a conventional diet without
N–EOs while the experimental groups received mixtures of N–EOs
based on soursop (S), lemon (L) and eucalyptus (E) in different
proportions: T1 (S: 33.4 , L:33.3%, E:33.3%), T2 (S:50%, L:25%,
E:25%), T3 (S:25%, L:50%, E:25%) and T4 ( S:25%, L:25%, E:50%).
The results showed that the T4 group showed the highest posture
rate compared to the T2 and T3 groups (P<0.05), although it was
similar to T0 and T1. Comparatively, the feed conversion was better
in the T4 treatment compared to T0 (P<0.05). The analysis of egg
quality showed that the T1 and T2 treatments reached a greater
shell thickness (mm) compared to the group with conventional diet
(P<0.05). The oxidative stability of the egg yolk evaluated through
the levels of malondialdehyde (MDA), showed that both the T1
and T4 groups had lower levels of MDA (P>0.05) compared to the
standard diet (T0). In conclusion, diets with N–EOs constitute a
promising option that favors feed conversion, laying percentage,
and greater shell thickness of the eggs of laying hens.
Key words: Laying hens; soursop; lemon; eucalyptus; productive
parameters
RESUMEN
Los aceites esenciales han demostrado efectos beneciosos en
los parámetros productivos de las aves de corral. Sin embargo, el
impacto de las mezclas de aceites esenciales nanoencapsulados
(N–EOs) en la dieta de las gallinas ponedoras ha sido poco descrito.
El objetivo de la investigación fue evaluar el efecto mezclas de
N–EOs en dietas de gallinas Lohmann Brown sobre el porcentaje
de postura, calidad y estabilidad oxidativa del producto huevo.
600 aves fueron distribuidas aleatoriamente en cinco grupos
(n=150 por grupo), según un diseño completamente al azar. El
grupo control recibió una dieta convencional no suplementada,
mientras que los grupos experimentales recibieron mezclas
de N–EOs a base de guanábana (S), limón (L) y eucalipto (E) en
diferentes proporciones: T1 (S:33,4 %; L:33,3 %; E:33,3 %); T2
(S:50 %; L:25 %; E:25 %); T3 (S:25 %; L:50 %; E:25 %) y T4 (S:25 %;
L:25 %; E:50 %). Los resultados mostraron que el grupo T4 tuvo
la mayor tasa de postura en comparación a los grupos T2 y T3
(P<0,05), aunque fue similar a T0 y T1. Comparativamente la
conversión alimenticia fue mejor en el tratamiento T4 con respecto
al T0 (P<0,05). El análisis de la calidad del huevo mostró que los
tratamientos T1 yT2 alcanzaron un mayor espesor de cascara
(mm),en comparación al grupo con dieta convencional (P<0,05).
La estabilidad oxidativa de la yema de huevo evaluada a través
de los niveles de malondialdehído (MDA), mostraron que tanto el
grupo T1 y T4 presentaban niveles más bajos de MDA (P>0,05)
en comparación a la dieta estándar (T0). En conclusión, dietas
con N–EOs constituyen una opción prometedora que favorece la
conversión alimenticia, el porcentaje postura, y un mayor espesor
de cáscara de los huevos de gallinas ponedoras.
Palabras clave: Gallinas de postura; guanábana; limón; eucalipto;
parámetros productivos
Effects of nanoencapsulated essential oil blend in diet of Lohmann
Brown hens on posture percentage, quality and egg oxidative stability
Efecto de la suplementación con una mezcla de aceites esenciales nanoencapsulados en dietas
de gallinas Lohmann Brown sobre el porcentaje de postura, calidad y estabilidad
oxidativa del huevo
Gilmar Mendoza–Ordoñez
1
* , Miguel Callacná–Custodio
1
, Vanessa Armas–Azabache
1
, Bruno Loyaga–Cortéz
1
,
Roberto Ybañez–Julca
2
, Daniel Asunción–Alvarez
2
, Hugo Saavedra–Sarmiento
1
, Aníbal Rodriguez–Vargas
3
1
Universidad Nacional de Trujillo, Facultad de Ciencias Agropecuarias, Laboratorio de Nutrición y Alimentación Animal. Trujillo, Perú.
2
Universidad Nacional de Trujillo, Facultad de Farmacia y Bioquímica, Laboratorio de Farmacología. Trujillo, Perú.
3
Universidad Nacional Daniel Alcides Carrión, Instituto de Investigación Especializada en Ganadería Oxapampa (INIGOX). Pasco, Perú.
*Corresponding author: gmendoza@unitru.edu.pe
Eects of nanoencapsulated essential oil blend in diet of Lohmann Brown hens / Mendoza-Ordoñez et al._______________________
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TABLE I
Experimental design for the inclusion of nanoencapsulated
essential oils (EOs) in feed, (% content in the composition)
Group Т0 Т1 Т2 Т3 Т4
Normal diet √ √ √ √ √
Soursop 0 33.4 50 25 25
Lemon 0 33.3 25 50 25
Eucalyptus 0 33.3 25 25 50
INTRODUCTION
Eggs have a diversity of nutrients such as essential lipids, proteins,
vitamins, minerals and trace elements of high digestibility and
accessible price, being a basic food in people’s diet. The egg industry
has been expanding in response to the rising demand for a safe,
reliable, and high–quality product. Therefore, the industry needs to
respond to the different challenges, perceptions and preferences of
consumers [1]. The increasing demand for animal protein has led
to intensied scientic advances in aviculture, such as the frequent
use of antibiotic growth promoters. These are used in constant
subinhibitory concentrations to limit the population of pathogenic
microorganisms in the intestinal microbiota [2]. Egg contamination
by microorganisms such as Salmonella spp., Escherichia coli,
Campylobacter jejuni and Listeria monocytogenes is possible,
generating different complications, the most serious of which is
the multi–resistance of these microorganisms to different antibiotics
[3]. This situation is the same for carcass/meat [4], manure and
soil fertilizer [5]. This situation poses a public health risk due to the
potential spread of resistance genes, highlighting the need to restrict
the non–therapeutic use of antibiotic growth promoters (AGP) [6].
Currently, consumer preferences are trending toward the
purchase of animal products raised without antibiotics. Hence,
there is a critical need for effective alternative growth promoters
and treatment methods (plant–derived products, organic acids,
probiotics, among others) for common poultry diseases [7]. Among
the new alternatives, the scientic evidence conrms that essential
oils (EO) have positive effects on the productive performance of
a variety of poultry such as quail (Coturnix coturnix japonica),
turkeys (Meleagris gallopavo), broilers or laying hens (Gallus gallus
domesticus), Peking ducks (Anas platyrhynchos), among others [8,
9, 10]. Essential oils mixtures of chemical compounds produced by
plants. They possess antibacterial, antifungal and antiviral activities
[11]. Evidence suggests that the use of EO alone or in combination
affects bird performance due to their effect on digestive processes,
although these results depend signicantly on the number and
type of birds [12, 13]. However, their action is limited due to their
volatile nature, reactivity and hydrophobicity. It is necessary to use
encapsulation methods to protect them [14]. Nanoencapsulation
emerges as a suitable method to preserve the stability, bioactivity
and bioavailability of bioactive agents, besides, it is a practical and
reproducible method [15]. In recent years, several studies have
reported that nanoencapsulation of EO, in addition to being a cost–
effective method for protecting bioactive compounds, also enhances
their benecial effects compared to EO in their free form [16, 17, 18].
However, despite these advances, there are few or no information
on the effects of nanoencapsulated essential oil (N–EOs) blends.
Therefore, the objective of the present study was to evaluate
the effects of dietary supplementation of nanoencapsulated EO
mixtures on production values, oxidative stability and egg quality
of laying hens.
MATERIALS AND METHODS
Experimental design and diets
The birds were handled in accordance with the guidelines of the
code of ethics for research of the Universidad Nacional de Trujillo.
A total of 600 20-week–old Lohmann Brown hens were randomly
assigned (completely randomized design) to ve dietary treatments
(T) with 5 replicates per treatment and 24 birds per replicate. During
the study, the birds were housed in metal cages (3.75 m
2
, Alaso
U.S.A. Corp., Florida, USA) on a local farm at a temperature 23 ± 3°C
and 82–90% humidity with a 12-h light regime. The control group
(T0) was fed a commercial diet without growth promoter, while the
other treatments (T1, T2, T3 and T4) received a diet supplemented
with a 75 mg·kg
-1
dose of nanoencapsulated EO–based mixture of
three local plants such as soursop (Annona muricata), lemon (Citrus
limon) and eucalyptus (Eucalytus globulus). A detailed description of
the treatments is described in TABLE I. The basal diet was formulated
according to the nutrient requirements of the Hy–line Brown user
manual [19]; feed components and nutrient compositions are shown
in TABLE II. Feed and water were provided ad libitum, and eggs
were collected at 8:00 am and 5:00 pm. Feeding, egg collection,
and egg weighing were performed daily for ten weeks.
Nanoencapsulation of essential oils
The EO of soursop seeds was obtained by the extrusion method.
Briefly, after collecting the soursop seeds, they were washed and
dried in an oven (SLN 15, Pol–Eko, Poland) at 70°C for two days,
then taken to a screw to be pressed (Oil Expeller, Mill Power, India)
at 100–105°C [20]. On the other hand, the essential oils of lemon
and eucalyptus leaves were extracted through steam distillation
(Essential oil extractor 04, Figmay, Argentina).
Once the oils were obtained, nanoencapsulation was carried
out as previously described [21] with some modications. The
modications included the use of casein as the aqueous phase
material, high–pressure homogenization with a microfluidizer (LM10,
Microfluidizer, USA), adjustment of the pH with HCl, and the use of
a Nano Spray Dryer (Laboratory Nano Spray Dryer, Techno Search
Process & Systems, India) for encapsulation. In detail, a primary
emulsion was obtained by mixing 18% (w/w) oil phase with 82%
(w/w) of a 4% casein aqueous phase at pH 7 using a high–speed
mixer (HG-15D, Witeg, Germany) for 30 s at the highest speed. This
pre–emulsion was then subjected to two passes of high shear fluid
homogenizer at room temperature (25°C) using a microfluidizer to
reduce the droplet size to nanometer levels. The primary emulsion
was then diluted, and the pH was adjusted with 0.3 N HCl to form
secondary emulsions. The interfacial double layer was formed by
diluting the secondary emulsions with the addition of maltodextrin
solutions to increase the solids content. Finally, nanocapsules of
mixtures of soursop, lemon and eucalyptus essential oil powders
were obtained by dehydration of secondary nanoemulsions by spray
drying using a Nano Spray Dryer.
Eects of nanoencapsulated essential oil blend in diet of Lohmann Brown hens / Mendoza-Ordoñez et al._______________________
_________________________________________________________________________________________________Revista Cientica, FCV-LUZ / Vol.XXXV
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TABLE II
Ingredients and nutrient composition of the experimental diets
Ingredients %
Corn 62.34
Soybean meal (48%) 15.80
Bran 4.60
Palm kernel meal 4.60
Calcium carbonate (0.85 – 2 mm) 2.50
Calcium carbonate (2 – 4 mm) 7.50
Dicalcium phosphate 0.80
Salt 0.25
Vegetable oil 1.00
Choline chloride 0.02
Lysine 0.05
Methionine 0.08
Enzyme complex 0.01
Sodium bicarbonate 0.20
Mycotoxin binder 0.15
Vitamin and mineral premix* 0.10
Nutrient Composition
Crude protein (%) 17.0
Metabolizable energy (Kcal·Kg
-1
) 3150.8
Phosphorus (%) 0.38
Calcium (%) 4.36
Methionine + Cysteine (%) 0.70
Methionine, Met (%) 0.40
Lysine, Lys (%) 0.84
*Per kg contains 8.000.000 IU vitamin A, 250.000 IU vitamin D3, 12.000 IU vitamin D,
1,8 g vitamin K3, 1 g vitamin B1, 4 g vitamin B2, 2,5 g vitamin B6, 0,025 g vitaminB12,
10 g vitamin B5, 0,5 g vitamin B9, 25 g vitamin B3, 80 g manganese, 72 g zinc, 55 g
iron, 10 g copper, 1 g iodine, 0,3 g selenium, and excipients. DM: Dry Matter
.
(Heidolph Instruments GmbH & Co, Germany) at 770 G for 30 s.
Then, it was centrifuged (Eppendorf, Centrifuge 5430R, Germany)
at 4435 G for 15 min at 4°C 1.5 mL of supernatant was taken
and added to 1.5 mL of 0.8% (w/v) aqueous 2-thiobarbituric acid
(TBA) 0.8% (w/v). Finally, this mixture was incubated (BINDER
GmbH, Model ED56, Germany) at 70°C for 30 min. The tubes were
cooled, and the reading was recorded at 532 nm (Fisher Scientic,
Microplate reader AccuSkan GO UV/Vis, USA).
Statistical analysis
To test the effect of dietary treatment, data on indicators of egg
quality and oxidative stability were analyzed by one–way ANOVA, as
appropriate. Differences between means were evaluated by Tukey’s
multiple comparisons test. A P≤0.05 was considered statistically
signicant. Values are expressed as the mean ± standard error of
the mean (SEM), and all statistical analyses were performed using
GraphPad Prism software (San Diego, CA, EE. UU.).
RESULTS AND DISCUSSION
Laying Performance
According to TABLE III, egg production rate was signicantly
increased in the T4 group compared to the T2 and T3 groups
(P<0.05), however, it was similar to the T0 and T1 groups. In
addition, the T4 treatment obtained a higher value of egg mass
than the control group (P<0.05) that received a non–supplemented
diet. The feed conversion was signicantly lower in T4 treatment
compared to the control and the T2 and T3 treatments (P<0.05).
Only the T1 group had a feed conversion rate that was statistically
comparable to that of the T4 group. (P>0.05). The feed intake,
weight gain, and egg weight were similar among all treatments
(P>0.05). Essential oils have been shown to possess bioactive
compounds with antibacterial, antifungal, antiparasitic and antiviral
activities [23]. Previously, Xiao et al. [24] showed that 300 mg·kg
-1
of a mixture of carvacrol, thyme and cinnamaldehyde in the diet
of laying hens did not signicantly affect egg production rate, feed
intake, egg weight and feed conversion ratio. This result does not
agree with this present research, where signicant differences
were found in egg production rate and feed conversion ratio. This
may be because nanoencapsulation increases the efciency of
production parameters by delivering the active compounds of the
EO directly to the absorptive cells of the small intestine mucosa
in a slow and controlled manner [25].
On the other hand, Eucalyptus powder has been reported to have
positive effects on production parameters such as egg production
rate, egg mass and feed conversion ratio in hens [26] as in quails
[27], showing that the treatment with the highest concentration
of eucalyptus EO has the best results. This could be attributed to
the fact that the active compounds of eucalyptus essential oil have
the ability to stimulate the secretion of digestive and pancreatic
enzymes [28]. Likewise, this effect could be enhanced by mixing
different essential oils [23].
Egg quality
The effects of supplementation of dietary N–EOs combinations
on egg quality indicators of laying hen eggs are shown in TABLE IV.
Treatments T1 and T2 were signicantly higher in eggshell thickness
Laying performance and egg quality
Eggs were collected daily and egg production rate was recorded for
a period of 21 to 30 weeks. During the experiment, egg weight and
mass were recorded daily. Feed intake was recorded daily, and the
feed conversion ratio rate was calculated. Each week, the live weight
of the hens was taken, and the daily weight gain was calculated.
In the nal week of the experiment, 30 eggs were randomly
selected daily from each treatment for a total of 210 eggs. The
eggs were used to determine fracture resistance, albumen height,
haugh unit, yolk color, yolk height, yolk diameter, yolk index and
shell thickness (Digital Egg Tester DET 6500, NABEL Co. Ltd.,
Kyoto, Japan).
Oxidative stability
The methodologies described by Loyaga–Cortéz et al. [9] and
Romero et al. [22] were used. Two grams (g) of egg yolk was
homogenized with 8.0 mL of 5% trichloroacetic acid in a vortex
Eects of nanoencapsulated essential oil blend in diet of Lohmann Brown hens / Mendoza-Ordoñez et al._______________________
4 of 7 5 of 7
TABLE III
Eects of nanoencapsulated EO supplementation on productive performance
Indicators
Treatments
P value
2
SEM
1
T0 T1 T2 T3 T4
Egg production rate (%) 76.78
ab
77.35
ab
72.44
b
75.37
b
81.13
a
0.004 0.825
Feed intake (hen·day
-1
·g
-1
) 109.19 109.22 109.17 109.19 109.17 1.000 0.148
Egg weight (g) 59.58 62.04 60.39 62.08 61.76 0.106 0.375
Feed conversion ratio 2.40
ab
2.32
bc
2.51
a
2.34
b
2.19
c
0.000 0.027
Egg mass (g·d
-1
) 55.76
bc
57.98
ab
53.73
c
56.78
abc
60.09
a
0.001 0.598
Weight gain (g·d
-1
) 2.17 3.86 2.88 2.89 3.68 0.385 0.293
Treatments include – Control group (T0): received a conventional diet. Experimental groups (T1-T4) received a diet supplemented with N–EO from soursop (S), lemon (L)
and eucalyptus (E) in dierent proportions (%).: T1 (S:33.4%, L:33.3% y E:33,3%), T2 (S:50%, L:25% y E:25%), T3 (S:25%, L:50% y E:25%) y T4: (S:25%, L:25% y E:50%).
a,b,c
Means
with dierent superscripts within the columns dier signicantly (
P<0.05).
1
SEM, standard error of the means.
2
P–value, signicance associated with dietary treatment
TABLE IV
Eects of nanoencapsulated EO supplementation on egg quality
Indicators
Treatments
P value
2
SEM
1
T0 T1 T2 T3 T4
Fracture resistance (kgf) 4.34 4.88 4.85 4.89 4.92 0.150 0.084
Albumen height (mm) 8.98 8.50 8.79 8.70 9.02 0.665 0.118
Haugh unit 94.26 93.16 92.42 91.71 93.33 0.708 0.758
Yolk color 6.29 6.02 6.18 5.95 6.02 0.395 0.060
Yolk height (mm) 18.02 18.01 18.05 18.59 18.27 0.295 0.099
Yolk diameter (mm) 39.76 41.82 40.42 40.37 39.81 0.601 0.429
Yolk index 0.47 0.44 0.46 0.46 0.46 0.223 0.010
Shell thickness (mm) 0.39
b
0.42
a
0.42
a
0.40
b
0.39
b
0.003 0.003
Treatments include – Control group (T0): received a conventional diet. Experimental groups (T1-T4) received a diet supplemented with N–EO from soursop (S), lemon (L)
and eucalyptus (E) in dierent proportions (%).: T1 (S:33.4%, L:33.3% y E:33,3%), T2 (S:50%, L:25% y E:25%), T3 (S:25%, L:50% y E:25%) y T4: (S:25%, L:25% y E:50%).
a,b
Means
with dierent superscripts within the columns dier signicantly (
P<0,05).
1
SEM, standard error of the means.
2
P–value, signicance associated with dietary treatment
than treatments T0, T3 and T4 (P<0.05). The supplementation of
different types of oil has increased shell thickness, except for the
treatments with a higher proportion of lemon and eucalyptus oil.
It has been reported that supplementation for 8 weeks of up to
3 g of Eucalyptus powder per kilogram of diet in laying hens has
no influence on shell thickness [26]. Also, supplementation of EO
blends of oregano, bay leaf oil, sage leaf oil, myrtle leaf oil, fennel
seed oil and citrus peel oil in laying hens has not shown signicant
effects on shell thickness [29, 30, 31].
Based on our findings, equal proportions of non–aromatic
essential oils enhance eggshell thickness, though this effect
is also observed with a higher proportion of essential oil from
soursop seed. To gain a better understanding of the metabolism of
essential oils, it is essential to identify their chemical composition
and primary deposition sites in the birds’ bodies. This would help
elucidate how nanoencapsulated essential oils (N–EOs) or their
metabolites contribute to the observed benets [32].
Oxidative stability
In addition to the production parameters, the oxidative stability
of egg yolk was studied in hens that received a diet supplemented
with the N–EOs mixture. As seen in FIG. 1, the control group
(T0) that received a standard diet showed the highest levels
of malondiandehyde (MDA), a marker of lipid peroxidation and
oxidative stress [33]. The T1 group that received equal parts N–
EOs supplementation (33.3%) showed a tendency to reduce MDA
levels compared to the control group (T1: 0.69 ± 0.01 nmol·L
-1
vs
T0 (control): 1.2 ± 0,23 nmol·L
-1
). This nding is consistent with
a previous study in which was reported that T1 treatment also
reduced lipid peroxidation in broiler thigh meat [18], however,
in the present study this difference did not reach the expected
statistical signicance (P>0.05). Similarly and following the same
trend as the T1 group, the T4 group presented lower MDA levels
compared to the control (0.78 ± 0.05 nmol·L
-1
; P>0.05).
It is widely known that poultry products are particularly prone
to oxidative deterioration due to their high concentrations of
polyunsaturated fatty acids, and EOs are a good alternative in
Eects of nanoencapsulated essential oil blend in diet of Lohmann Brown hens / Mendoza-Ordoñez et al._______________________
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T0 T1 T2 T3 T4
0.0
0.5
1.0
1.5
2.0
2.5
MDA levels (nmol·L
-1
)
FIGURE 1. Eect of nanoencapsulated EOs supplementation on oxidative stability
of egg yolk. Control group (T0): received a conventional diet. The experimental
groups (T1-T4) received a diet supplemented with N–EOs from soursop (S), lemon
(L) and eucalyptus (E) in dierent proportions (%): T1 (S:33.33%, L:33.33% and
E:33.33%), T2 (S:50%, L:25% and E:25%), T3 (S:25%, L:50% and E:25%) and T4:
(S:25%, L:25% and E:50%). Each circle represents an individual value (n)
this context [32]. In this study, the addition of N–EOs to the diet
maintained a tendency to reduce the concentration of MDA in egg
yolk of laying hens. EO from Eucalyptus globulus has been described
to reduce serum MDA levels in broiler chickens [28], probably due
to its radical scavenging properties and also the ability to inhibit
lipid peroxidation [34]. The main component of eucalyptus EOs
is the terpene 1,8-cineole, also known as eucalyptol [34], has
been shown to improve total antioxidant activity in broilers by
reducing MDA levels and increasing total superoxide dismutase
enzyme activity [35].
In addition, compounds such as δ–cadinene, α–muurolene, β–
caryophyllene, epic–α–cadinol and α–cadinol present in Annona
muricata L. (Soursop) EO [36], as well as, d–Limonene and β–Pinene
present in Citrus limon EO [37] could contribute to this antioxidant
effect. The individual or synergistic effects of all these compounds
present in each of the EOs used have a tendency to reduce of
lipid peroxidation in egg yolk. Fortication of foods with bioactive
compounds such as EOs serves to improve the quality characteristics
of derived products and protects consumers against oxidation [38].
CONCLUSION
In conclusion, the ndings in this study indicate that dietary
supplementation with nanoencapsulated essential oil (N–EO)
blends signicantly improves feed conversion efciency, boosts
egg production rates, and enhances eggshell thickness in laying
hens. Furthermore, N–EOs contribute to reduced lipid peroxidation
in egg yolk, although this reduction was not signicant. These
results suggest that incorporating N–EOs into poultry diets could
be a valuable strategy for optimizing the health and productivity
of laying hens.
ACKNOWLEDGMENTS
This research was supported by The National Program for
Scientic Research and Advanced Studies (Prociencia – Peru)
under the framework of the “Project for the Improvement and
Expansion of the Services of the National Science, Technology, and
Technological Innovation System,” grant number N°010-2020.
Conflict of interests
The authors declare no conflicts of interest.
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