Livestock Science 191 (2016) 117124

Contents lists available at ScienceDirect

Livestock Science
journal homepage: www.elsevier.com/locate/livsci

The effect of dietary supplementation of the broiler chicken diet with

Boswellia serrata resin on growth performance, digestibility, and
gastrointestinal characteristics, morphology, and microbiota
B. Kiczorowska a,n, A.R.M. Al-Yasiry a,b, W. Samoliska a, A. Marek c, E. Pyzik c
a

Institute of Animal Nutrition and Bromatology, University of Life Science, Lublin, Poland
Department of Animal Resources, University of Wasit, Al Kut, Wasit, Iraq
c
Sub-Department of Preventive Veterinary and Avian Diseases, Institute of Biological Bases of Animal Diseases, Faculty of Veterinary Medicine, University of
Life Science, Lublin, Poland
b

art ic l e i nf o

a b s t r a c t

Article history:
Received 30 September 2015
Received in revised form
25 July 2016
Accepted 25 July 2016

The study was conducted to determine the effect of supplementation of the broiler chicken diet with
Boswellia serrata resin (BSR) on growth performance, dry matter, organic matter, and energy digestibility,
as well as gastrointestinal characteristics, morphology, and microbiota. A total of 200 one-day-old broiler
chickens were assigned randomly to 4 treatments with 5 replicate cages of 10 broiler chickens per cage (5
females and 5 males). The experiment lasted 6 wk, and broiler chickens were fed diets containing 0
(control), 3 (BSR3), 4 (BSR4), or 5% Boswellia serrata resin (BSR5). There was no effect of the treatments on
growth performance. The proportion of the proventriculus in the metabolic weight was lower (quadratic,
P o0.05) in the broiler chickens fed the diets containing BSR compared to those fed the control diet. In
addition, broiler chickens fed the BSR3 and BSR4 diets had greater digestibility of dry matter and organic
matter (control vs. BSR diets and quadratic, Po 0.05). The jejunum was shorter (P o0.05) in broiler
chickens fed the diets supplemented with BSR (control vs. BSR diets and quadratic, P o0.05). In the
duodenum of chickens receiving BSR diets, a decrease in the depth of crypts and an increase in the villus:
crypt were observed (quadratic, P o 0.05). In broiler chickens fed the BSR diets, a decrease in the count of
Escherichia coli and an increase in the count of Lactobacillus and Enterococcus were observed (control vs.
BSR diets and quadratic, P o0.05). A decreased count of Clostridium spp. strains was observed as well
(control vs. BSR diets and linear, P o0.05). The resin of Boswellia serrata can be considered as a good feed
additive, which can have positive effects on intestinal microbiota and the gastrointestinal tract morphology of broiler chickens.
& 2016 Elsevier B.V. All rights reserved.

Keywords:
Broiler chicken
Boswellia serrata resin
Growth performance
Digestibility
Gastrointestinal characteristics

1. Introduction
Controlling intestinal functions and inuencing the condition
of gastrointestinal microbiota by means of feed additives has been
long considered the main tool for improving the production performance and health status of animals. A majority of poultry in
industrial production were stimulated by supplementation of
synthetic substances to enhance their production performance or
therapy (Flanders and Gillespie, 2016; Laxminarayan et al., 2015).
The ban on using antibiotics as feed additives accelerated research
and led to intense studies of alternative feed additives in poultry
production. One such alternative is phytogenic feed additives including herbs, spices, or resins containing a diet of various
n

Corresponding author.
E-mail address: bozena.kiczorowska@up.lublin.pl (B. Kiczorowska).

http://dx.doi.org/10.1016/j.livsci.2016.07.019
1871-1413/& 2016 Elsevier B.V. All rights reserved.

aromatic compounds and volatile substances. These supplements

improve the health status in broiler chickens and their production
performance, among other things, by stimulating the microbiota of
the gastrointestinal tract or improving the digestibility of nutrients
(Abdel-Wareth et al., 2012; Cho et al., 2014). Generally, they are
believed to be safe and are approved for marketing by the FDA
(2016) and for animal production in Europe following registration
with the EURFA (2016).
Feed additives approved for use in poultry production (EURFA,
2016) include the resin of Boswellia serrata (referred to as frankincense or olibanum), which is exotic in the European market.
Frankincense comes from the Arabian Penninsula, where it is obtained from trees from the Burseraceae family (Thulin and Warfa,
1987). This traditional medicine of the East is believed to have an
anti-inammatory, antiseptic, and even anticancer or anxiolytic
effect (Dharmananda, 2003; Van Vuuren, 2008). These therapeutic
properties are associated with the presence of many aromatic

118

B. Kiczorowska et al. / Livestock Science 191 (2016) 117124

2. Materials and methods

hen house allowed controlling the length of light exposure during

the day according to the guidelines on rearing of broiler chickens
(Aviagen, 2014a).
The basal feed diets were made from cereal meal middlings
(wheat and corn) and post-extraction soybean meal as recommended (Aviagen, 2014b) (Table 1). The broiler chickens were
fed 3 types of diets: starter 021 d), grower 2135 d), and nisher
3542 d). The starter diet was fed to the broiler chickens in a
crumbled form, and the grower and nisher diets in a granulated
form. The resin was obtained from Boswellia serrata trees by incision of a bark-less trunk and left to dry in natural conditions
(direct information from the seller). Fragmented natural Boswellia
serrata resin (BSR) was obtained commercially (Baghdad, Iraq).
Dietary treatments consisted of the control and the control supplemented with 3 (BSR3), 4 (BSR4), or 5% BSR (BSR5). All the diets
were iso-energetic and iso-nitrogenous.

2.1. Animals and dietary treatments

2.2. Growth performance

The experiment was carried out after approval by the Second

Local Ethics Committee at the University of Life Sciences in Lublin
(No. 27/2014). Two hundred broiler chickens (Ross 308, Aviagen,
Cracow, Malopolska, Poland) were allocated to cages, and the cages were randomly assigned to 4 dietary treatments with 5 cages
per treatment and 5 females and 5 males per cage. The initial body
weight of the broiler chickens was 42.8 70.2 g. The experiment
lasted 6 wk. The broiler chickens were reared in 1-m2 cages, provided with continuous access to feed and water, in a room with
controlled temperature and humidity. The lighting scheme in the

The body weight of each broiler chicken and the feed intake
were recorded at 0, 10, 21, 35, and 42 d of life. Body weight gains
and feed conversion ratio (FCR) were calculated for each period.
Mortality rates were recorded daily, and the weight of dead broiler
chickens were used to adjust average daily gain (ADG), average
daily feed intake (ADFI), and FCR.
Feed digestibility was evaluated by the indicator method (with
internal markers acid-insoluble ash), and 4 broiler chickens were
selected randomly from each cage at the nal nisher stage
(Kussaibat and Leclercq, 1985). The content of dry matter and

substances among which the highly active boswellic acid is predominant (Camarda et al., 2007). The therapeutic capabilities of
Boswellia have been conrmed by many researchers and well
documented in literature (Huang et al., 2000; Schrott et al., 2014;
Siddiqui, 2008; Umar et al., 2014; Zhao et al., 2003). However,
there is no information about its suitability for use in poultry
production and the effect of such supplementation on the production traits and health status of broiler chickens. Therefore, the
aim of the study was to determine the effect of 3 different levels of
Boswellia serrata resin supplementation in diets for broiler chickens on the fundamental production traits, dry matter, organic
matter, and energy digestibility, as well as the structure of the
gastrointestinal tract and its microbiological condition.

Table 1
Dietary ingredients and the nutrient content of the experimental diets (as-fed basis).
Item

Dietsa
Starter (021 d)

Grower (2135 d)

Finisher (3542 d)

BSR3

BSR4

BSR5

BSR3

BSR4

BSR5

BSR3

BSR4

BSR5

Ingredients, %
Wheat
Soybean meal, 46% CPb
Maize
Boswellia serrata (resin)
Soybean oil
Dicalcium phosphate
Limestone
NaCl
DL-Metc
L-Lysd
Vitamin-mineral premixe

20.0
39.47
30.0

6.0
1.8
1.2
0.33
0.36
0.34
0.5

20.0
38.47
30.0
3.0
4.0
1.8
1.2
0.33
0.36
0.34
0.5

20.0
39.47
28.0
4.0
4.0
1.8
1.2
0.33
0.36
0.34
0.5

20.0
39.47
27.0
5.0
4.0
1.8
1.2
0.33
0.36
0.34
0.5

23.0
36.76
29.0

7.0
1.8
1.0
0.5
0.33
0.36
0.25

23.0
36.76
28.0
3.0
5.0
1.8
1.0
0.5
0.33
0.36
0.25

23.0
37.26
27.0
4.0
4.5
1.8
1.0
0.5
0.33
0.36
0.25

23.0
37.26
26.0
5.0
4.5
1.8
1.0
0.5
0.33
0.36
0.25

26.0
32.13
30.0

8.0
1.8
0.7
0.5
0.33
0.34
0.2

26.0
31.13
30.0
3.0
6.0
1.8
0.7
0.5
0.33
0.34
0.2

26.0
31.13
29.0
4.0
6.0
1.8
0.7
0.5
0.33
0.34
0.2

26.0
31.13
28.0
5.0
6.0
1.8
0.7
0.5
0.33
0.34
0.2

Chemical composition
MEnf, MJ/kg
CP, g/kg
Lys, g/kg
Met Cys, g/kg
Ca, g/kg
P, g/kg
Na, g/kg

12.55
212.2
13.81
10.53
9.67
5.79
1.68

12.55
211.9
13.79
10.48
9.54
5.69
1.73

12.55
212.4
13.84
10.54
9.59
5.76
1.75

12.55
212.6
13.76
10.51
9.63
5.85
1.74

12.97
192.1
12.91
9.83
8.74
5.31
1.71

12.97
192.8
12.84
9.76
8.67
5.33
1.69

12.97
193.4
12.86
9.86
8.65
5.41
1.65

12.97
193.5
12.95
9.81
8.73
5.38
1.74

13.39
185.4
11.36
9.03
7.93
3.93
1.76

13.39
185.5
11.33
8.94
7.95
3.98
1.62

13.39
185.9
11.41
9.11
7.88
3.79
1.78

13.39
185.6
11.45
9.08
7.96
4.01
1.64

a
Treatments: C control diet without Boswellia serrata reisn (BSR) supplementation; BSR3 diet with 3% BSR supplementation; BSR4 diet with 4% BSR supplementation; BSR5 diet with 5% BSR supplementation.
b
CP crude protein.
c
Evonik Degussa Gmbh, Essen, Germany (per kilogram of 990 g Met).
d
Ajinomoto Eurolysine S.A.S., Amiens. France (per kilogram of 780 g Lys).
e
Added minerals and vitamins per kg of starter diet: Mn, 100 mg; I, 1 mg; Fe, 40 mg; Zn, 100 mg; Se, 0.15 mg; Cu, 10 mg; vitamin A, 15,000 IU; vitamin D3, 5000 UI;
vitamin E, 75 mg; vitamin K3, 4 mg; vitamin B1, 3 mg; vitamin B2, 8 mg; vitamin B6, 5 mg; vitamin B12, 0.016 mg; biotin, 0.2 mg; folic acid, 2 mg; nicotic acid, 60 mg;
pantothenic acid, 18 mg; choline, 1800 mg. Added minerals and vitamins per kg of grower diet: Mn, 100 mg; I, 1 mg; Fe, 40 mg; Zn, 100 mg; Se, 0.15 mg; Cu, 10 mg; vitamin A,
12,000 IU; vitamin D3, 5000 UI; vitamin E, 50 mg; vitamin K3, 3 mg; vitamin B1, 2 mg; vitamin B2, 6 mg; vitamin B6, 4 mg; vitamin B12, 0.016 mg; biotin, 0.2 mg; folic acid,
1.75 mg; nicotic acid, 60 mg; pantothenic acid, 18 mg; choline, 1600 mg. Added minerals and vitamins per kg of nisher diet: Mn, 100 mg; I, 1 mg; Fe, 40 mg; Zn, 100 mg; Se,
0.15 mg; Cu, 10 mg; vitamin A ,12,000 IU; vitamin D3, 5000 UI; vitamin E, 50 mg; vitamin K3, 2 mg; vitamin B1, 2 mg; vitamin B2, 5 mg; vitamin B6, 3 mg; vitamin B12,
0.011 mg; biotin, 0.05 mg; folic acid, 1.5 mg; nicotic acid, 35 mg; pantothenic acid, 18 mg; choline, 1600 mg; and
f
MEn metabolizable energy (ME) in the diets corrected to zero nitrogen balance.

B. Kiczorowska et al. / Livestock Science 191 (2016) 117124

organic matter was determined in the collected droppings (AOAC,

2000), and the content of nitrogen was determined according to
Ekman et al. (1949). The dry matter and organic matter digestibility coefcient and the content of nitrogen-corrected metabolizable energy (MEn) were calculated for each diet (WPSA, 1986).
2.3. Chemical analysis and gastrointestinal characteristics
The content of total protein in the diets was determined (AOAC,
2000) and the actual content of Men was calculated (WPSA, 1986).
The amino acid contents were determined using an automatic
amino acid analyzer (AAA 400; Ingos, Prague, Czech Republic)
after previous acid hydrolysis with 6 M HCl (method 994.12; AOAC,
2000). Cysteine and Met were determined after oxidative hydrolysis (Arnoldi, 2001). Samples of the feed were dried at 100 C for
24 h and ashed for 10 h at 550 C. The ashed samples were dissolved in a nitric acid-perchloric acid diet (1:1) and diluted with
deionized water for mineral analysis. Contents of Na and Ca were
measured using ame atomic absorption spectrophotometry
(Unicam 939/959AA-6300; Shimadzu Corp., Tokyo, Japan), according to the Polish Standard (Polish Committee for Standardization, 2002), and total P content was determined colorimetrically
(Polish Committee for Standardization, 1976) with a spectrophotometer (Helios Alpha UVvis; Spectronic Unicam, Leeds,
United Kingdom).
One female and 1 male broiler chickens with the body weight
close to the average were selected from each cage to determine
gastrointestinal characteristics. Dissection analysis was carried out
according to the method described by Zioecki and Doruchowski
(1989), during which the gastrointestinal tract was separated and
the weight of the proventriculus and gizzard were determined.
Additionally, the lengths of the duodenum, jejunum and the total
intestinal length were measured. The weight of empty organs was
expressed relative to metabolic body weight (MBW), which is
dened as body weight raised to the 0.75 power (BW0.75).
Samples of the intestines after separation were xed in Bouin's
solution (Gabe, 1976), dehydrated, and parafn-embedded. Longitudinal, 6-7-m thick, consecutive parafn sections were prepared and stained with hematoxylineosin (HE) (Zawistowski,
1986). Morphometric analyses were performed on the duodenum
and jejunum of 10 broiler chickens per treatment. The preparations were analyzed under a light microscope (Axio Imager; Carl
Zeiss MicroImaging GmbH, Gttingen, Germany). Patches with a
correct structure were scanned (Mirax Desk scanner; Carl Zeiss
Microscopy GmbH, Jena, Germany). The measurements of the intestinal structures were performed using image analysis program
(Zeiss Axiovision LE ver. 4.1.; Zeiss MicroImaging GmBH). The
height of the mucous layer, villus height, and crypt depth were
measured, and the villus height to crypt depth ratio was then
calculated. Five measurements of each structure were performed
per sample. The villus height was measured from the tip of the
villus to the villus-crypt junction, while the crypt depth was dened as the depth of the invagination between adjacent villi.
2.4. Microbiological analysis
The 3 samples of the small intestine collected during the dissection were weighed, diluted with phosphate buffered saline
(PBS), and homogenized (Stomacher BagMixer 400; Interscience,
Breda, the Netherlands). Next, the supernatant samples were xed
for 16 h at 4 C in paraformaldehyde (Sigma-Aldrich, Warsaw,
Poland) (Fuchs et al., 2007). The resultant suspension was homogenized again with glass balls (3 mm) for 5 min (Merck, Darmstadt, Germany). Using centrifugation (5000  g for 5 min at 4 C),
eukaryotic cells and undigested food were removed (MPW-350R;
MPW Medical Instruments, Warsaw, Poland). The resultant

119

supernatant was placed on white polycarbonate membrane lters

(pore size0.2 mm) (Milipore, Cork, Ireland) by means of sterile
lter units (Nalgene, Lima, OH, US). Samples for further analyses
were stored at a temperature of  20 C.
In the uorescent in situ hybridization method, microorganisms were determined using group-specic probes (Thermo Scientic, Ulm, Germany): for Bacteria domain, Eub338 5GCTGCCTCCCGTAGGAGT-3, for Lactobacillus-Enterococcus, Lab151
5 GGTATTAGCA/TCTGTTTCCA, for Bidobacterium sp., Bif164 5CATCCGGCATTACCACCC, and Non- Eub338 5-CGACGGAGGGCATCCTCA-3 as a negative control.
The total count of Lactobacillus, Enterococcus, and Bidobacterium was identied using lysozyme diluted in TE-His buffer
(100 mM Tris[hydroxymethyl]aminomethane hydrochloride [Tris
HCl] [pH 8.0], 50 mM EDTA) placed on a membrane lter. After
incubation for 10 min at room temperature, the lters were dried
and dehydrated in ethanol. The 10 L of hybridization buffer (5 M
NaCl, 20 mM Tris HCl, formamide in respective concentrations,
distilled water, and 0.01% sodium dodecyl sulfate [SDS]) with indocarbocyanine (Cy3) at a concentration of 50 ng/L were placed
on the lters. Depending on the type of bacteria identied, hybridization was carried out for 90 min at a temperature of 46 C or
for 24 h at 35 C. The remains were ushed with the buffer
(900 mM NaCl, 20 mM Tris HCl, 5 mM EDTA, distilled water, 0.01%
SDS) in a water bath at a temperature of 48 C or 37 C for Grampositive bacteria. The samples were ushed with distilled water,
dried at room temperature, stained with a DAPI solution (4-6diamidino-2-phenylinole) at a concentration of 1 mg/mL (Porter
and Feig, 1980), and covered with Citiuor and Vectashield immersion oils (4:1). The samples were covered with slips and stored
at  20 C for further microscopic analyses. The stained preparations were analyzed using an epiuorescent microscope (Olympus
BX51; Olympus Optical Co., Ltd., Tokyo, Japan) by means of lters
(BP 360370 nm lter, DM 400 nm, BA 420 nm) and appropriate
software (Olympus Cell F; Olympus Poland, Warsaw, Poland).
The count of Escherichia coli, Clostridium spp., and Salmonella
sp. in the intestines was determined by culturing colonies. The
3 samples of the small intestine, including fragments of the intestine from the bile duct outlet to Meckel's diverticulum and from
Meckel's diverticulum to the outlets of the ceca, weighed 10 g
each. The samples were placed in sterile stomacher bags (400 mL),
suspended in 90 mL of 0.1% sterile buffered peptone water
(CM0509; OXOID, Thermo Scientic, Lenexa, KS, US), and homogenized (Stomacher BagMixer 400; Interscience, Breda, the
Netherlands).
Escherichia coli was determined on EMB Agar, Levine medium
(E022; Biomaxima S.A. Centre for Microbiology Emapol, Gdask,
Poland). The dishes were incubated at a temperature of 37 C for
24 h in an aerobic environment. To conrm the species, the selected colonies from each diluted sample were subjected to API
20E biochemical testing (BioMrieux Poland Sp. z o.o., Warsaw,
Poland).
The microbial count of Escherichia coli was determined according to the formula:
C
L (N1 +0.1N2) d x a , where: C total colonies in all dishes selected

for counting; N1number of dishes from the rst counted dilution; N2 number of dishes from the second counted dilution;
d dilution ratio corresponding to the rst (lowest) counted dilution ratio of material quantity, for 0.1 cm3 culture; and a 10.
The count of Clostridium spp. was determined using the Fung
double tube (FDT) method developed by Fung and Lee (1980). One
vial of the SFP supplement (Biomaxima S.A. Centre for Microbiology Emapol) with kanamycin sulfate and polymyxin B sulfate
and 25 mL of Egg Yolk Emulsion (EM 045; Biomaxima S.A. Centre
for Microbiology Emapol) were added to 500 mL of SFP agar base

120

B. Kiczorowska et al. / Livestock Science 191 (2016) 117124

The broiler chickens covered by the study consumed similar

amounts of feed and achieved similar BW, ADG, and FCR (Table 2).
A low mortality rate, i.e. one dead broiler chicken, was found only
in treatment BSR5.
The introduction of Boswellia serrata into broiler chicken diets

resulted in changes in the morphology and functioning of the

gastrointestinal tract. Broiler chickens fed with diet with BSR had a
lower share in MBW of the proventriculus compared to the control
treatment (P o0.05), with a quadratic pattern (P o0.05) (Table 3).
The length of the duodenum increased quadratically (P o0.05) in
broiler chickens fed with diet supplemented with BSR. A shorter
jejunum was characteristic of broiler chickens fed diet with BSR
compared to the control treatment (Po 0.05), and this effect decreased quadratically (P o0.05).
The length of the duodenum, the jejunum, and the total intestinal length were linearly negatively correlated with the proportion of the BSR in the diets (rs  0.59,  0.44, and 0.70 for
BSR3, BSR4, and BSR5, respectively). Consequently, better digestive
efciency of dry matter (P o0.05) and organic matter (P o0.05)
was noted in the BSR treatments and increased digestibility
quadratically (P o0.05).
As a result of supplementing the diet with BSR, slight morphometric changes occurred in the walls of the small intestine of
broiler chickens (Table 4). The effect was dependent on the dose of
the resin. In the histological samples of the duodenum of chickens
receiving the largest content of Boswellia serrata (BSR5) in the diet,
an quadratic increase in the depth of crypts and a decrease in the
villus: crypt were observed (Po 0.05). The coefcients of Spearman's rank correlation between the BSR applied dose and histomorphometric ratios of the wall of the small intestine had low
values. The results indicate an insignicant relationship between
the addition of BSR to the diet and the examined characteristics of
the small intestine of broiler chickens.
The supplementation of the feed diets for broiler chickens with
BSR had a signicant effect on the intestinal microbiota. The addition of BSR in the diets resulted in a quadratic increase in the
presence of the following strains in the intestines of the broiler
chickens: Bacteria (Po0.05), Lactobacillus, and Enterococcus
(P o0.05) compared to the control (C) (Table 5). Only the population of Bidobacterium, regardless of the type of the diet, remained at the same level in all chicks covered by the study. No
Salmonella sp. bacteria were found in any study material. In the
case of Clostridium perngers, regardless of the intestinal section
(to Meckels diverticulum and from Meckels diverticulum), and in
the case of the total count of bacteria (P o0.05) a linear decrease in
their population (P o0.05) was observed but only after using the
4% and 5% BSR supplementation the feed diets for chickens. A
decrease in the Escherichia coli count was only found in the BSR5
treatment, which was conrmed by the quadratic value of the
effect (Po 0.05).

Table 2
Average body weight (BW), average daily feed intake (ADFI), average daily gain
(ADG), and feed conversion ratio (FCR) in broiler chickens.a

4. Discussion

(Biomaxima S.A. Centre for Microbiology Emapol) sterilized in an

autoclave. The prepared base was placed into sterile tubes with a
diameter of 1.5 cm, 25 mL each, and the test culture was maintained in a water bath at a temperature of 45 C. Next, the tested
material was transferred into tubes with the SFP base. The tubes
were incubated at a temperature of 37 C for 2448 h in an
anaerobic environment. The microbial count of Clostridium spp. in
the tested samples was determined according to the formula:
C
L (N1 +0.1N2) d , where: C total colonies in all tubes selected for
counting; N1number of tubes from the rst counted dilution;
N2 number of tubes from the second counted dilution; and
d dilution ratio corresponding to the rst (lowest) counted
dilution.
To conrm the species, the colony from each dilution was selected and examined with biochemical tests (RapID ANA II System;
Thermo Scientic) and the results were read by means of database
(ERIC Web; Thermo Scientic). In the intestine samples, isolation
was performed to determine the presence of Salmonella sp. on a
poorly selective MacConkey medium (OXOID; Thermo Scientic)
and a strongly selective SS medium (OXOID; Thermo Scientic).
The dishes were incubated at a temperature of 37 C for 24 h.
2.5. Statistical analysis
Each cage was used as an experimental unit. The data obtained
were developed by the ANOVA method using one-way analysis of
variance ( 95; P o0.05) and calculating the mean values for the
groups ( x ) and the standard error of the mean (SEM). Linear and
quadratic polynomial contrasts were used to evaluate the effects of
different dietary levels of Boswellia serrata resin. The direction and
intensity of the relationships between the level of Boswellia seratta
addition and the productivity, histomorphometric, and microbiological measurements were performed using Spearman's rank
correlation coefcients (rs). The signicance of differences was
determined with Statistica 10.0 software (StatSoft Inc., 2011).

3. Results

Item

BW, g

ADFI, g/kg ADG, g/

chicken

FCR,
kg/kg

Mortality of
chickens, heads

Initial Final
Treatments
C
BSR3
BSR4
BSR5
SEM

43.0
42.8
42.6
42.7
1.8

2526
2539
2537
2390
19

102.9
103.2
102.3
100.6
1.6

56
59
59
57
o 1

1.73
1.67
1.68
1.78
0.04

0
0
0
1

P-value
C vs. BSR
Linear
Quadratic

0.721
0.963
0.831

0.728
0.953
0.637

0491
0.788
0.578

a
Data represent the mean of 5 cages (10 broiler chickens/cage) per treatment;
SEM standard error of the means; and C control diet without Boswellia serrata
reisn (BSR) supplementation; BSR3 diet with 3% BSR supplementation;
BSR4 diet with 4% BSR supplementation; BSR5 diet with 5% BSR supplementation.

The diet addition of the Boswellia serrata resin did not exert an
effect on the FCR values in the broiler chickens covered by the
study. The use of phytogenic feed additives, and in particular
therapeutic plants, in animal production improves production efciency. This phenomenon is also observed in the case of both
traditional European herbs (Basmacolu et al., 2004; Florou-Paneri et al., 2006) and phytobiotics (herbs, Asian mushrooms, resins) sourced from outside Europe (Guo et al., 2004; Landy et al.,
2011; Nadeem, 2012). However, excessive doses of phytobiotics
with strong bioactivity such as the Boswellia serrata resin can inhibit animal weight gain. This was observed in treatment BSR5.
Singh et al. (2008) obtained similar results in their studies of rats,
where a dose amounting to 500 mg/kg of body weight was sufcient to inhibit their growth.
The effect of the supplementation with the BSR was also observed in the development of respective elements of the gastrointestinal tract of the broiler chickens. Broiler chickens fed diet

B. Kiczorowska et al. / Livestock Science 191 (2016) 117124

121

Table 3
Indices of gastrointestinal development in broiler chickens at d 42.a
Item

MBW, kg

Stomach

Length of small intestine, cm/kg MBW

Digestibilityb, g/kg

Proventriculus, MBW %

Gizzard, MBW %

Duodenum

Jejunum

Total

Dry matter

Organic matter

Energy

Treatments
C
BSR3
BSR4
BSR5
SEM

0.356
0.357
0.357
0.341
0.012

1.24
1.10
1.11
1.23
0.03

6.32
6.07
6.46
6.49
0.07

20.81
22.56
21.57
19.84
0.78

55.91
54.34
52.42
51.98
1.45

164.6
169.5
168.4
155.4
5.6

0.804
0.843
0.832
0.784
0.009

0.801
0.852
0.841
0.819
0.015

0.798
0.805
0.813
0.784
0.011

P-value
C vs. BSR
Linear
Quadratic

0.856
0.854
0.772

0.042
0.453
0.037

0.227
0.552
0.048

0.421
0.321
0.029

0.039
0.255
0.021

0.589
0.911
0.255

0.034
0.132
0.013

0.011
0.156
0.042

0.783
0.825
0.671

a
Data represent the mean of 5 cages (2 broiler chickens/cage) per treatment; SEM standard error of the means; MBW metabolic body weight, which is dened as
body weight raised to the 0.75 power (BW0.75); C control diet without Boswellia serrata reisn (BSR) supplementation; BSR3 diet with 3% BSR supplementation; BSR4 diet
with 4% BSR supplementation; BSR5 diet with 5% BSR supplementation; and
b
Data represent the mean of 5 cages (4 broiler chickens/cage) per treatment.

Table 4
Morphometric measurements of the small intestine mucosa of broilers chicken at d 42.a
Item

Duodenum

Jejunum

Mucosa thickness, mm

Crypt depth, mm

Villus height, mm

Villus: crypt

Mucosa thickness, mm

Crypt depth, mm

Villus height, mm

Villus: crypt

Treatments
C
BSR3
BSR4
BSR5
SEM

2151
2091
2110
2227
75

355.8
330.9
311.0
401.3
13.3

1993
2088
2110
1968
58

5.65
6.39
6.80
4.90
0.30

2082
1789
1999
2022
88

374.7
376.8
347.0
414.8
11.9

1802
1829
1837
1795
74

4.86
4.85
5.31
4.28
0.19

P-value
C vs. BSR
Linear
Quadratic

0.487
0.757
0.624

0.268
0.234
0.022

0.179
0.930
0.382

0.145
0.410
0.023

0.246
0.972
0.431

0.432
0.388
0.177

0.167
0.987
0.848

0.263
0.445
0.181

a
Data represent the mean of 5 cages (2 broiler chickens/cage) per treatment; SEM standard error of the means; C control diet without Boswellia serrata reisn (BSR)
supplementation; BSR3 diet with 3% BSR supplementation; BSR4 diet with 4% BSR supplementation; BSR5 diet with 5% BSR supplementation; and Villus:crypt villi
length to the depth of the crypts.

with the BSR content showed a lower proportion of the proventriculus in the MBW; however, this did not reduce the digestive
efciency, in particular that of dry and organic matter. The intensity of digestion is determined by the level of secretion of hydrochloric acid and pepsinogen and the frequency of exchange of
the digesta between the proventriculus and the gizzard. The proventriculus is also a place where mineral salts, and mainly Ca and
P, are dissolved (Jamroz et al., 2006). Gupta et al. (2001) report that

the supplementation of the diet with the Boswellia serrata resin

increases the absorption of iron, calcium, and phosphorus, which
can also contribute to improved digestibility of dry matter and
organic matter in feed. Excessive development of the proventriculus and the gizzard leads to intestinal reux, due to which the
digesta is repeatedly exposed to hydrochloric acid and pepsinogen
(Amerah and Ravindran, 2008; Hetland et al., 2004; Svihus, 2011;
Wu and Ravindran, 2004). However, the results of the present

Table 5
Bacteria identied in the intestinal contents of broiler chickens at d 42.a
Item

Bacterial counts per g of intestinal contents (log10)

Total count

Bacteria

Lactobacillus and Enterococcus

Bidobacterium sp.

Escherichia coli

Salmonella sp.

Clostridium perfringers
Jejunum

Ileum

Treatments
C
BSR3
BSR4
BSR5
SEM

9.65
9.58
9.44
8.78
0.46

8.57
9.33
9.28
8.37
0.08

7.79
8.45
8.37
8.14
0.05

8.12
8.57
8.84
8.78
0.06

6.60
6.25
6.35
5.65
0.10

ND
ND
ND
ND

4.90
4.60
4.00
3.85
0.07

5.45
5.25
4.90
4.95
0.05

P-value
C vs. BSR
Linear
Quadratic

0.033
0.037
0.014

0.026
0.334
0.033

0.018
0.532
0.038

0.543
0.110
0.523

0.048
0.272
0.036

0.039
0.018
0.548

0021
0.025
0.481

a
Data represent the mean of 5 cages (2 broiler chickens/cage) per treatment; SEM standard error of the means; C control diet without Boswellia serrata reisn (BSR)
supplementation; BSR3 diet with 3% BSR supplementation; BSR4 diet with 4% BSR supplementation; BSR5 diet with 5% BSR supplementation; and ND non detected.

122

B. Kiczorowska et al. / Livestock Science 191 (2016) 117124

studies do not clearly conrm such a relationship. Control broiler

chickens, despite having the largest stomachs, did not achieve the
best digestibility results. Similarly, it seems that the 5% supplementation of the diet (BSR5) is too high to achieve satisfactory
production performance. The observations show, on the other
hand, that the nal efciency of nutrient digestion is equally affected by factors such as the length of intestines and their physical
condition as well as the microbiological environment. The supplementation of 3% and 4% of BSR contributed to an increase in the
length of the duodenum. The small intestine of poultry is of great
importance for digestion and absorption of nutrients. Liver enzymes emulsifying fats and pancreatic enzymes hydrolyzing fats
(pancreatic lipase), carbohydrates (pancreatic alphaamylase), and
proteins (trypsin and chymotrypsin) are secreted into the duodenum (Adil et al., 2010; Shih and Hsu, 2006). Qurishi et al. (2010)
report that boswellic acid stimulates secretion of pancreatic enzymes, thus improving protein and energy digestibility and reducing endogenous losses of nitrogen as well as production of
ammonia and other microbial metabolites. On the other hand,
Dzubak et al. (2006) report its stimulating effect on liver function.
In their studies involving mice and guinea pigs, Borrelli et al.
(2006) show that supplementation of feed with the Boswellia
serrata resin normalizes intestinal peristalsis, reduces the pH of
the digesta, improves intestinal passage of the digesta, has a
trophic effect on the mucosa of the digestive tract, and prevents
diarrhea. Krieglstein et al. (2001) conrm that resins of the Boswellia type stimulate digestive functions, reduce gases, and enhance the ow of digestive juices. The results of the present studies indicate that the best conditions for dry matter and organic
matter digestion in the gastrointestinal tract were created in
broiler chickens fed diets with 3% and 4% of BSR addition.
The use of phytobiotic additives in animal nutrition can contribute to enhancement of the function of the entire gastrointestinal tract, including increased integrity of the epithelial
barrier of the intestines providing protection against pathogenic
microbiota (Jamroz et al., 2005; 2006; Windisch et al., 2009). The
positive changes in the small intestine were observed in the experimental treatments BSR3 and BSR4. The changes were probably
connected with the antibacterial properties of the resin. Boswellia
serrata used in broiler chicken feeding contains a number of
bioactive components (-boswellic acid, acetyl--boswellic acid,
11-keto--boswellic acid, and 3-O-acetyl-11-keto--boswellic
acid), exerts an anti-inammatory and antibacterial effect, and
stabilizes intestinal functions (Aman et al., 2010; Anthoni et al.,
2006; Borrelli et al., 2006; Camarda et al., 2007; Raja et al., 2011).
The 3% and 4% BSR diet addition positively modied the composition of the intestinal microbiota, increasing the share of the desirable strains of Lactobacillus and Enterococcus and reducing the
count of Clostridium spp., which becomes virulent easily. The
changes in the bacterial count in the intestine can have a positive
effect on its histomorphometry, activity of intestinal enzymes,
digestion and absorption processes, metabolism of the components and, as a result, contribute to better production performance. Such a positive effect was observed in broiler chickens
treatments BSR3 and BSR4. It is commonly believed that the
structure of intestinal mucosa can provide information about the
health status of the gastrointestinal tract. Stress factors related to
poor nutrition and health status of animals can lead to negative
changes in intestinal mucosa manifested by shortening of villi and
simultaneous deepening of the crypts. As a result, the total absorptive surface area of the intestine is considerably decreased and
thus the absorption of nutrients is reduced, which is directly reected in deteriorated production performance (Perry, 2006).
Despite the fact that the antibacterial effect of phytobiotics is
well known and has been supported by many studies (Franz et al.,
2010; Jamroz et al., 2005; Kommera et al., 2006; Manzanilla et al.,

2004; Sivroopoulou et al., 1996; Tiihonen et al., 2010), reference

literature contains many ambiguous reports concerning the effect
(or lack of the effect) of these additives on the histomorphometry
of animal intestines (Abdel-Rahman et al., 2014; Jamroz et al.,
2006; Manzanilla et al., 2004; Zeng et al., 2015). Since the higher
(BSR5) share of resin in the diet increased the depth of crypts of
Lieberkhn in the duodenum, it appears not to have been optimal.
Windisch et al. (2009) emphasize that one of the negative aspects
of phytogenic additives such as essential oils (EOs) can be the irritation of intestinal tissue leading to a decrease in the intestine's
absorptive surface area. On the other hand, they may have a positive impact on intestinal health since they reduce the number of
pathogens, which stimulates an increase in villus length and intestinal surface area. It seems that the general effect of phytogenic
additives on intestinal morphology will depend on the dose and
balance between potential irritation of intestinal tissue and the
positive effect on the function and integrity of the intestinal
mucosa.
Many researchers report strong antibacterial properties of the
resin of Boswellia serrata thanks to the content of verticilla-4 (20),
7,11-trien and incensol, acetyl-keto-boswellic acid and -, -BA
3-oxo-tirucallic acids (Mothana et al., 2011). A strong antibacterial
effect of Boswellia serrata was observed after the application of its
various forms and doses: a petroleum ether-based extract
against Staphylococcus aureus (Raja et al., 2011) and an acetonebased extract against Eschericha coli and Klebsiella pneumoniae
(Rajendra et al., 2013). The results in the present studies conrm
this information. A strong negative correlation was observed between the total bacterial count in the intestines of chickens
(rs  0.76) and strains that easily become virulent, e.g. Escherichia
coli and Clostridium spp., and the amount of BSR supplementation
(rs  0.93 and 0.92, respectively). However, a greater antibacterial effect of BSR was observed in the intestines of broiler
chickens in treatments BSR4 and BSR5 (Po 0.05). Patel and Patel
(2014) conrm that Boswellia serrata resin used in the disc diffusion method, regardless of the form in which it is applied (extracts
based on water, petroleum ether, acetone, and methanol), shows a
high zone of inhibition against Escherichia coli and Clostridium spp.
Similar results were also obtained by Bushra et al. (2012), who
carried out studies involving 35-D-old hen broilers. Miklaeli et al.
(2003) report a benecial effect of Boswellia serrata, due to its
antibacterial properties, on the stabilization of the microbiota in
the gastrointestinal tract. It is also associated with a reduction of
pH in the intestinal tract. Such conditions are conducive to the
growth of Lactobacillus and Enteroccocus strains. The BSR diet addition, particularly with the 3% and 4% content, may have stimulated the growth of the colonies of these bacteria in the intestines
of broiler chickens.

5. Conclusions
The use of the 3% and 4% addition of the Boswellia serrata resin
in the diets increased the digestibility of dry matter and organic
matter in the feed. In addition, the histomorphometry of the small
intestine suggests a benecial effect of the addition these levels of
Boswellia serrata on the architecture of the mucosa. The BSR used
in the diets had a stabilizing effect on the bacterial ora of the
gastrointestinal tract by decreasing the count of Escherichia coli
and Clostridium spp. strains, but on the other hand increasing the
count of Lactobacillus and Enterococcus. To sum up, the resin of
Boswellia serrata can be considered as a good feed additive, which
can have positive effects on intestinal microbiota and the gastrointestinal tract morphology of broiler chickens.

B. Kiczorowska et al. / Livestock Science 191 (2016) 117124

Conict of interest
The authors declare no conicts of interest.

References
Abdel-Rahman, H.A., Helal, M.A., Nafeaa, A.A., Zahran, I.S., 2014. Effect of turmeric
(Curcuma longa), fenugreek (Trigonella foenum-graecum L.) and/or bioavonoid
supplementation to the broiler chicks diet and drinking water on the growth
performance and intestinal. Glob. Vet. 12, 627635.
Abdel-Wareth, A.A.A., Kehraus, S., Hippenstiel, F., Sdekum, K.H., 2012. Effects of
thyme and oregano on growth performance of broilers from 4 to 42 days of age
and on microbial counts in crop, small intestine and caecum of 42-day-old
broilers. Anim. Feed Sci. Technol. 178, 198202.
Adil, S., Banday, T., Bhat, G.A., Mir, M.S., Rehman, M., 2010. Effect of dietary supplementation of organic acids on performance, intestinal histomorphology, and
serum biochemistry of broiler chicken. Vet. Med. Int. . http://dx.doi.org/
10.4061/2010/479485, Accessed 10 April 2016
Aman, M., Ravishankar Rai, V., Samaga, P.V., 2010. Antimicrobial and phytochemical
screening of Boswellia serrata Roxb., Rhus mysorensis Heyne, Strychnos potatorum Linn. F. and Schefera stellata Gaertn. Med. Aromat. Plant Sci. Biotechnol.
4, 6972.
Amerah, A.M., Ravindran, V., 2008. Inuence of method of whole-wheat feeding on
the performance, digestive tract development and carcass traits of broiler
chickens. Anim. Feed Sci. Technol. 147, 326339.
Anthoni, C., Laukoetter, M.G., Rijcken, E., Vowinkel, T., Mennigen, R., Mller, S.,
Senninger, N., Russell, J., Jauch, J., Bergmann, J., Granger, D.N., Krieglstein, C.F.,
2006. Mechanisms underlying the anti-inammatory actions of boswellic acid
derivatives in experimental colitis. Am. J. Physiol. Gastrointest. Liver Physiol.
290, 11311137.
AOAC, 2000. Ofcial Methods of Analysis. 17th (ed.) Assoc. Off. Anal. Chem. Int.,
Gaithersburg, MD, US.
Arnoldi, A., 2001. Thermal processing and foods quality: analysis and control. In:
Richardson, P. (Ed.), Thermal Technologies in Food Processing. Woodhead
Publishing, Cambridge, UK, pp. 138159.
Aviagen, 2014a. Ross 308 broiler: Nutrition specications. http://en.aviagen.com/
assets/Tech_Center/Ross_Broiler/Ross308BroilerNutritionSpecs2014-EN.pdf
(accessed 10.04.16).
Aviagen, 2014b. Ross broiler management handbook. http://en.aviagen.com/assets/
Tech_Center/Ross_Broiler/Ross-Broiler-Handbook-2014i-EN.pdf (accessed
10.04.16).
Basmacolu, H., Tokuolu, ., Ergl, M., 2004. The effect of oregano and rosemary
essential oils or alpha-tocopheryl acetate on performance and lipid oxidation of
meat enriched with n-3 PUFAs in broilers. S. Afr. J. Anim. Sci. 34, 197210.
Borrelli, F., Capasso, F., Capasso, R., Ascione, V., Aviello, G., Longo, R., Izzo, A.A., 2006.
Effect of Boswellia serrata on intestinal motility in rodents: inhibition of diarrhoea without constipation. Br. J. Pharmacol. 148, 553556.
Bushra, S.R., Zangana, A.S.A., Alyasery, A.R.M., 2012. Efcacy evalution of adding
levels of frankincense (Boswellia carteri) to drinking water on some body dimensions and intestinal microora in gut of broiler chicks. J. Biol. Chem. Environ. Sci. 6, 431444.
Camarda, L., Dayton, T., Di Stefano, V., Pitonzo, R., Schillaci, D., 2007. Chemical
composition and antimicrobial activity of some oelegum resin essential oil from
Boswellia spp. (Burseraceae). Ann. Chim. 97, 837844.
Cho, J.H., Kim, H.J., Kim, I.H., 2014. Effects of phytogenic feed additive on growth
performance, digestibility, blood metabolites, intestinal microbiota, meat color
and relative organ weight after oral challenge with Clostridium perfringens in
broilers. Livest. Sci. 160, 8288.
Dharmananda, S., 2003. Myrrh and frankincense. The Institute for Traditional. Med.
Prev. Health Care http://itminfoeu.businesscatalyst.com/assets/myrrh.pdf
(accessed 11.04.16).
Dzubak, P., Hajduch, M., Vydra, D., Hustova, A., Kvasnica, M., Biedermann, D.,
Markowa, L., Urban, M., Sarek, J., 2006. Pharmacological activities of natural
triterpenoids and their therapeutic implications. Nat. Prod. Rep. 23, 394411.
Ekman, P., Emanuelson, H., Fransson, A., 1949. Investigations concerning the digestibility of protein in poultry. K. Lantbr. Ann. 16, 749776.
EURFA, 2016. European Union Register of Feed Additives pursuant Regulation (EC)
No 1831/2003. Annex I: List of additives. Eddition 227, page 95. http://ec.
europa.eu/food/food/animalnutrition/feedadditives/docs/comm_register_feed_
additives_183103.pdf (accessed 10.04.16).
FDA, 2016. Food and Drug Administration. Food and drugs. Food and drug administration, Department of Health and Human services (chapter I). Animal
drugs, feeds, and related products (subchapter E). Substances Generally Recognized as Safe (part 582). U.S. Government Online Bookstore. http://www.
ecfr.gov/cgi-bin/text-idx?
SID 66dc623ca208c4629f07f54feac3a2c1&mc true&tpl /ecfrbrowse/Ti
tle21/21cfrv6_02.tpl#0 (accessed 11.04.16).
Flanders, F., Gillespie, J., 2016. Modern Livestock & Poultry Production, 9th ed.
Cengage Learning, Independence, KY, US.
Florou-Paneri, P., Giannenas, I., Christaki, E., Govaris, A., Botsoglou, N.A., 2006.
Performance of chickens and oxidative stability of the produced meat as affected by feed supplementation with oregano, vitamin C, vitamin E and their
combinations. Arch. Geugel. 70, 232240.

123

Franz, C., Baser, K.H.C., Windisch, W., 2010. Essential oils and aromatic plants in
animal feeding a European perspective. A review. Flavour Frag. J. 25, 327340.
Fuchs, B.M., Pernthaler, J., Amann, R., 2007. Single cell identication by uorescence
in situ hybridization. In: Reddy, C.A. (Ed.), Methods for General and Molecular
Microbiology, 3rd ed. ASM Press, Washington, DC, US, pp. 886896.
Fung, D.Y.C., Lee, C.M., 1980. Double-tube anaerobic bacterial cultivation system.
Food Sci. 7, 209213.
Gabe, M., 1976. Histological Techniques. Springer-Verlag, New York, US.
Guo, F.C., Williams, B.A., Kwakkel, R.P., Li, H.S., Li, X.P., Luo, J.Y., Li, W.K., Verstegen,
M.W., 2004. Effects of mushroom and herb polysaccharides, as alternatives for
an antibiotic, on the caecal microbial ecosystem in broiler chickens. Poult. Sci.
83, 175182.
Gupta, I., Parihar, A., Malhotra, P., Gupta, S., Ludtke, R., Safayhi, H., Ammon, H.P.T.,
2001. Effects of gum resin of Boswellia serrata in patients with chronic colitis.
Planta Med. 67, 391395.
Hetland, H., Choct, M., Svihus, B., 2004. Role of insoluble non-starch polysaccharides in poultry nutrition. Worlds Poult. Sci. J. 60, 415422.
Huang, M.T., Badmaev, V., Ding, Y., Liu, Y., Xie, J.G., Ho, C.T., 2000. Anti-tumor and
anti-carcinogenic activities of triterpenoid, beta-boswellic acid. Biofactors 13,
225230.
Jamroz, D., Wiliczkiewicz, A., Wertelecki, T., Orda, J., Skorupiska, J., 2005. Use of
active substances of plant origin in chicken diets based on maize and locally
grown cereals. Br. Poult. Sci. 46, 485493.
Jamroz, D., Wertelecki, T., Houszka, M., Kamel, C., 2006. Inuence of diet type on the
inclusion of plant origin active substances on morphological and histochemical
characteristics of the stomach and jejunum walls in chicken. J. Anim. Physiol.
Anim. Nutr. 90, 255268.
Kommera, S.K., Mateo, R.D., Neher, F.J., Kim, S.W., 2006. Phytobiotics and organic
acids as potential alternatives to the use of antibiotics in nursery pig diets.
Asian-Australasian. J. Anim. Sci. 19, 17841789.
Krieglstein, C.F., Anthoni, C., Rijcken, E.J., Laukptter, M., Spiegel, H.U., Boden, S.E.,
Schweizer, S., Safayhi, H., Senninger, N., Schurmann, G., 2001. Acetyl-11-ketobboswellic acid, a constituent of a herbal medicine from Boswellia serrata resin,
attenuates experimental ileitis. Int. J. Colorectal Dis. 16, 8895.
Kussaibat, R., Leclercq, B., 1985. A simplied rapid method for the determination of
apparent and true metabolizable energy values of poultry feed. Arch. Geugel.
49, 5462.
Landy, N., Ghalamkari, Gh, Toghyani, M., 2011. Performance, carcass characteristics,
and immunity in broiler chickens fed dietary neem (Azadirachta indica) as alternative for an antibiotic growth promoter. Livest. Sci. 142, 305309.
Laxminarayan, R., Van Boeckel, T., Teillant, A., 2015. The Economic Costs of Withdrawing Antimicrobial Growth Promoters from the Livestock Sector, OECD
Food, Agriculture and Fisheries Papers, No. 78, OECD Publishing. http://dx.doi.
org/10.1787/5js64kst5wvl-en (accessed 11.04.16).
Manzanilla, E.G., Perez, J.F., Martin, M., Kamel, C., Baucells, F., Gasa, J., 2004. Effect of
plant extracts and formic acid on the intestinal equilibrium of early-weaned
pigs. J. Anim. Sci. 82, 32103218.
Miklaeli, B.R., Maatooq, G.T., Badria, F.A., Amer, M.M.A., 2003. Chemistry and immunomodulatory activity of frankincense oil. Z. Nat. C. 58, 230238.
Mothana, R.A.A., Hasson, S.S., Schultze, W., Mowitz, A., Lindequist, U., 2011. Phytochemical composition and in vitro antimicrobial and antioxidant activities of
essential oils of three endemic Soqotraen Boswellia species. Food Chem. 3,
11491154.
Nadeem, S., 2012. Synergistic effect of Commophora mukul (gum resin) and Lagenaria siceraria (fruit) extracts in high fat diet induced obese rats. Asian Pac. J.
Trop. Dis. 2, 883886.
Patel, N.B., Patel, K.C., 2014. Antibacterial activity of Boswellia serrata Roxb. ex Colebr, Ethanomedicinal Plant Against Gram Negative UTI Pathogens, LSL. 53, 97
1098.
Avian gut function in health and disease. In: Perry, G.C. (Ed.), Poultry Science
Symposium Series. CABI Publishing, UK.
Porter, K.G., Feig, Y.S., 1980. The use of DAPI for identifying and counting aquatic
microora. Limnol. Oceanogr. 25, 943948.
Polish Committee for Standardization, 2002. Polish Standard PN-EN ISO 6869,
Animal Feeding Stuffs Determination of the Contents of Calcium, Copper, Iron,
Magnesium, Manganese, Potassium, Sodium and Zinc Method Using Atomic
Absorption Spectrometry. Warsaw, Poland.
Polish Committee for Standardization, 1976. Polish Standard PN-76/R-64781, Feed.
Determination of Phosphorus Content (in Polish). Warsaw, Poland.
Qurishi, Y., Hamid, A., Zargar, M.A., Singh, S.K., Saxena, A.K., 2010. Potential role of
natural molecules in health and disease: importance of boswellic acid. J. Med.
Plants Res. 4, 27782785.
Raja, A.F., Ali, F., Khan, I.A., Shawl, A.S., Arora, D.S., Shah, B.A., Taneja, S.C., 2011.
Antistaphylococcal and biolm inhibitory activities of acetyl-11-keto-- boswellic acid from Boswellia serrata. BMC Microbiol. 11, 5467.
Rajendra, C.E., Harish, K.D.H., Yeshoda, S.V., Mahaboob, A.N., Hanuman, T., 2013.
Comparative evaluation of antimicrobial activities of methanolic extract of
Curcuma longa and Boswellia serrata. Int. J. Res. Pharm. Chem. 3, 22312781.
Schrott, E., Laufer, S., Lmmerhofer, A., Ammon, H.P.T., 2014. Extract from gum resin
of Boswellia serrata decreases [IA.sub.2]-antibody in a patient with Late onset
Autoimmune Diabetes of the Adult (LADA). Phytomedicine 21, 786794.
Shih, B.L., Hsu, J.C., 2006. Development of the activities of pancreatic and caecal
enzymes in White Roman goslings. Br. Poult. Sci. 47, 95102.
Siddiqui, M.Z., 2008. Boswellia serrata, a potential antiinammatory agent: an
overview. Indian J. Pharm. Sci. 73, 255261.
Singh, S., Khajuria, A., Taneja, S.C., Khajuria, R.K., Singh, J., Johri, R.K., Qazi, G.N.,

124

B. Kiczorowska et al. / Livestock Science 191 (2016) 117124

2008. The gastric ulcer protective effect of boswellic acids, a leukotriene inhibitor from Boswellia serrata, in rats. Phytomedicine 15, 408415.
Sivroopoulou, A., Papanikolaou, E., Nikolaou, C., Kokkini, S., Lanaras, T., Arsenakis,
M., 1996. Antimicrobial andcytotoxic activities of oreganum essential oils. J. Agr.
Food Chem. 44, 12021205.
StatSoft, Inc., 2011. STATISTICA (data analysis software system), version 10. www.
statsoft.com.
Svihus, B., 2011. The gizzard: function, inuence of diet structure and effects on
nutrient. Worlds Poult. Sci. J. 67, 207224.
Thulin, M., Warfa, A.M., 1987. The frankincense trees (Boswellia spp., Burseraceae) of
northern Somalia and southern Arabia. Kew Bull. 42, 487500.
Tiihonen, K., Kettunen, H., Bento, M.H.L., Saarinen, M., Lahtinen, S., Ouwehand, A.C.,
Schulze, H., Rautonen, N., 2010. The effect of essential oils on broiler performance and gut microbiota. Br. Poult. Sci. 51, 381392.
Umar, S., Umar, K., Sarwar, A.H.M.G., Khan, A., Ahmad, N., Ahmad, S., Katiyar, C.K.,
Husain, S.A., Khan, H.A., 2014. Boswellia serrata extract attenuates inammatory
mediators and oxidative stress in collagen induced arthritis. Phytomedicine 21,
847856.
Van Vuuren, S.F., 2008. Antimicrobial activity of South African medicinal plants. J.
Ethnopharmacol. 119, 462472.
Windisch, W., Rohrer, E., Schedle, K., 2009. Phytogenic feed additives to young

piglets and poultry: mechanisms and application. In: Steiner, T. (Ed.), Phytogenics in Animal Nutrition: Natural Concepts to Optimize Gut Health and
Performance. Nottingham University Press, Nottingham, UK, pp. 1939.
WPSA, 1986. World's Poultry Science Association. European Table of Energy Values
for Poultry Feedstuffs. 1st (ed.) Subcommittee Energy of the Working Group no.
2. Nutrition of the European Federation of Branches of the WPSA. Wageningen,
the Netherlands.
Wu, Y.B., Ravindran, V., 2004. Inuence of whole wheat inclusion and xylanase
supplementation on the performance, digestive tract measurements and carcass characteristics of broiler chickens. Anim. Feed Sci. Technol. 116, 129139.
Zawistowski, S., 1986. Histological Technique, Histology and Histopathology Basis
(in Polish), 5th ed. PCWL, Warsaw, Poland.
Zeng, Z., Xu, X., Zhang, Q., Li, P., Zhao, P., Li, Q., Piao, X., 2015. Effects of essential oil
supplementation of a low-energy diet on performance, intestinal morphology
and microora, immune properties and antioxidant activities in weaned pigs.
Anim. Sci. J. 86, 279285.
Zhao, W., Entschladen, F., Liu, H., Niggemann, B., Fang, Q., Zaenker, K.S., Han, R.,
2003. Boswellic acid acetate induces differentiation and apoptosis in highly
metastatic melanoma and brosarcoma cells. Cancer Detect. Prev. 27, 6775.
Zioecki, J., Doruchowski, W., 1989. The Method of Assessment of Slaughter Poultry
(in Polish). COBRD Publishing, Pozna, Poland.