JWPR  
Poultry Research  
J. World Poult. Res. 10(2S): 184-194, June 14, 2020  
Journal of World’s  
Research Paper, PII: S2322455X2000024-10  
License: CC BY 4.0  
Comparative Clinicopathological Study of Salmonellosis in  
Integrated Fish-Duck Farming  
Anwaar M. El-nabarawy1, Mohamed A. Shakal2, Abdel-Haleem M. Hegazy3 and Mohamed M. Batikh4*  
1 Poultry Disease Department- Faculty of Veterinary Medicine-Cairo University, Egypt  
2 Poultry Disease Department- Faculty of Veterinary Medicine-Cairo University, Egypt  
3 Poultry Disease Department Animal Health Research Institute-Kafr El-Sheikh Provisional Lab, Egypt  
4 Poultry Disease Department Animal Health Research Institute-Kafr El-sheikh Provisional Lab, Egypt  
*Corresponding author’s Email: anwaar.elnabarawy@gmail.com; ORCID: 0000-0003-1618-6842  
Received: 13 Feb. 2020  
Accepted: 23 Mar. 2020  
ABSTRACT  
Poultry litter is used in fish farms as fertilizer thus integrated fish-duck farming is common in some areas of Egypt.  
Salmonella bacteria may be present in poultry litter and contaminate fish ponds and infect duck farms. To investigate  
incidence and prevalence of Salmonella infection in integrated duck-fish farms, 50 litter samples, 200 cloacal swabs  
from integrated duck farms, 60 liver samples from integrated duck farms and 69 water samples from the fish pond  
were collected. Results revealed the isolation and identification of 19 Salmonella spp. belonging to 14 different  
serotypes (4 isolates from litter, 2 isolates from fish pond water, 8 isolates from cloacal swabs of ducks and 5 isolates  
from ducks liver). Fifty, one-day-old Pekin ducks were experimentally infected with five chosen Salmonella  
serotypes (S. Bargny, S. Tshingwe, S. Uganda, S. Kentucky, and S. Enteritidis). The results from experimental  
infection revealed clinicopathological findings including degeneration and necrosis in the liver, lymphoid depletion  
and macrophage infiltration in the spleen and enteritis. Mortality ranged from 28.6% in S. Bargny, S. Enteritidis and  
S. Kentucky and increased to 42.9% in S. Uganda and reached up to 100% in S.Tshingwe. Body weight gain  
decreased by 16% in S. Uganda and exceeded to 23.9% in S. Kentucky and decreased by 31% in S. Bargny and S.  
Enteritidis as compared to the control group. Feed conversion ratio was recorded and ranged from 5.1, 5.11, 4.98,  
5.15 and 4.02 in S. Bargny, S. Uganda, S. Kentucky, S. Enteritidis, and control group, respectively. In conclusion,  
different species of Salmonella can affect integrated duck-fish farms and cause high mortality as well as a decrease in  
feed intake, feed conversion ratio, and body weight gain.  
Key words: Histopathology, Integrated duck-fish farms, Pathogenicity, Salmonella spp.  
pathogens in litter and in the aqua-system is considered  
one of the critical reasons for infection transmission (Guan  
INTRODUCTION  
Some of the fish farms are integrated with waterfowl as  
integrated duck-fish farms are preferred as ducks fit easily  
into aquaculture facilities, inducing, vegetation, pest  
control, and fertilization roles, in the same time this  
system needs minimum requirement concerning facilities  
and expenditure in this warm water system (Little and  
Edwards, 2003; Majhi, 2018). Poultry litter is used by  
some farms as a fertilizer due to the non-digested feed,  
metabolic excretory products and residues in poultry litter  
resulting in a microbial synthesis that can be utilized to  
replace reasonable parts of feedstuff used in conventional  
2017). The microbiological examination of poultry litter  
exhibits various pathogenic microorganisms. Existence of  
The objective of the present study was to identify  
Salmonella species which may be present in poultry litter  
and can access to fish ponds during fertilization of the  
ponds and consequently infect ducks integrated with  
aquaculture. Moreover, the clinicopathological aspects of  
salmonellosis were evaluated by experimental infection of  
ducklings with isolated Salmonella.  
MATERIALS AND METHODS  
Ethical approval  
The animal use protocol in this study approved by  
the Institutional Animal Care and Use Committee  
(Vetcu02122019102).  
To cite this paper: El-nabarawy AM, Shakal MA, Hegazy AM and Batikh MM (2020). Comparative Clinicopathological Study of Salmonellosis in Integrated Fish-Duck Farming.  
184  
J. World Poult. Res., 10(2S): 184-194, 2020  
ducklings subdivided into six equal groups (1-6) by  
Experimental design and sampling  
Samples were obtained according to the research  
design from the different districts in Kafr El-Sheikh  
Governorate, Egypt. In total, 50 litter samples, 200 cloacal  
swabs from integrated duck farms and 69 water samples  
from fish ponds, 60 liver samples were taken from  
sacrificed ducks from different fish farms. All samples  
were labeled and transported to the laboratory. (Animal  
Health Research Institute, Kafr El-Sheikh provisional  
laboratory, Egypt). The samples were subjected to  
Salmonella isolation and identification.  
ranking methods. At the 7th day, the first five groups were  
inoculated orally (using 1-ml sterile feeding tube via crop)  
9
containing (1x10 cfu) / duckling (Barrow et al., 1999) of  
each of S. Bargny, S. Tshingwe, S. Uganda, S. Kentucky,  
and S. Enteritidis respectively, while the 6th group kept as  
uninfected control and was similarly inoculated orally with  
physiological saline. Each group was reared separately in  
wire-floored batteries and fed on commercial ration which  
contain the nutritional requirement for Pekin duckling.  
Feed and water were given ad.lib. All ducklings were kept  
under observation for signs and deaths up to 3 weeks of  
age. Cloacal swabs were collected for detection of fecal  
shedding from all groups during the first 3 days post-  
inoculation (PI), then at the weekly interval at the 2nd and  
the 3rd week PI. Moreover, at the end of the 2nd and 3rd  
week, two randomly selected ducks were sacrificed from  
each group for postmortem, bacteriological and  
histopathological examination. Initial and final body  
weight, feed consumption, body weight gain and feed  
conversion rate were calculated at a weekly interval as  
averages. Percentages of the average values of the infected  
groups were also calculated relative to the average values  
of the uninfected control group to allow better comparison.  
Also Re-isolation of salmonellae from dropping, liver,  
spleen and gall bladder of experimentally infected seven-  
day-old ducklings.  
Isolation and identification of different  
Salmonella serotypes  
Isolation of different Salmonella was applied on  
litter. Briefly, 25 g of litter samples were prepared by  
mixing in a sterile flask with 225 ml phosphate buffer  
saline (PBS, Bio Basic, Canada). Water samples obtained  
through inverting a 500 ml sterilized flask in 30 cm (Abd-  
Elghany et al., 2015) depth water surface. Then, 30 ml of  
water samples were clarified by centrifugation (centrifuge-  
Universal- Germany) at 5000 rpm for 5 minutes. Cloacal  
swabs and liver samples (A sterile cotton swabs stabbed  
into liver parenchyma) by using nutrient broth (Oxoid,  
UK), where 1 ml of all of these samples inoculated in  
nutrient broth and incubated at 37ºC for 24 hr. Then, 1 ml  
of incubated broth was inoculated into selenite F broth  
(Oxoid, UK) and incubated at 37 ºC for 24 hr. a loopful  
from this broth were streaked onto Salmonella-shigella  
(SS) agar (Oxoid, UK) and incubated at 37 ºC for 24 hr.  
All the suspected pure colonies of salmonellae were  
furtherly subjected to biochemical reactions (methyl-red,  
Voges-Proskauer, indole and urea tests) according to  
Cheesbrough (1985). Biochemically positive reaction for  
Salmonella isolates was finally identified according to  
(Grimont and Weill, 2007) using Salmonella poly ”O”  
antiserum and Salmonella monovalent ”O and H”  
antiserum (SINIF Co., Germany). Then a five Salmonella  
isolates were employed to study the clinicopathological  
picture in duckling.  
Statistical analysis  
The obtained numerical data were statistically  
analyzed using SPSS software. Duncan's multiple range  
test was used for testing significance of differences among  
group means at p-value<0.05.  
RESULTS  
Results of salmonellae isolation are shown in table 1,  
which revealed that 19 Salmonella isolates were recorded  
from poultry litter, fish pond water, cloacal swabs of  
integrated ducks and liver of integrated ducks at rates of 8,  
2.9, 4 and 8.3%, respectively.  
Comparative clinicopathological effects of  
Salmonella isolates  
All 19 Salmonella isolates were subjected to  
biochemical identification and the results are summarized  
and presented in table 2. The biochemically identified  
Salmonella isolates were serologically identified by using  
monovalent and polyvalent "O" and "H" Salmonella  
antisera. Results are summarized and presented in tables 3  
and 4. Nineteen Salmonella isolates included S. Kentucky  
Fifty, one-day-old Pekin duckling were employed to  
study the clinicopathological effects of the different  
Salmonella isolates including S. Bargny, S. Tshingwe, S.  
Uganda, S. Kentucky and S. Enteritidis in susceptible one-  
week-old ducklings through oral inoculation. Eight  
experimental ducklings were bacteriologically examined  
and proved to be free from Salmonella. The remaining 42  
185  
El-nabarawy et al., 2020  
(n=4), S. Enteritidis (n=2), S. Bargny (n=2) and one  
groups. Mortality ranged from 28.6% in S. Bargny, S.  
Enteritidis and S. Kentucky and increased to 42.9% in S.  
Uganda and reached up to 100% in S.Tshingwe as  
mentioned and recorded in table 6.  
isolate for each of S. Belgdam, S. Cuckmere, S.  
Tshiongwe, S. Gueuletapee, S. Oxford, S. Atakpame, S.  
Ferruch, S. Uganda, S. Amsterdam, S. Brikama and S.  
Kulsrivier. Salmonella Kentucky was the most frequent  
isolate with a rate of 21%, followed by S. Enteritidis and  
S. Bargny with a rate of 10.5%. Table 4 shows that all  
Salmonella isolated were motile containing flagellar  
antigen "H" with its two phases "H1" and "H2" except S.  
Belgdam, S. Gueuletapee, S. Amsterdam and S. Enteritidis  
which contained "H1" only.  
Also shedding pattern (Table 7), organ colonization  
(Table 8), initial body weight, final body weight, feed  
consumption, body weight gain, and feed conversion rate  
(Table 9) were measured and calculated.  
Histopathological findings in ducklings infected  
with salmonellae  
Generally, Salmonella infection in ducklings  
produced marked tissue alterations as compared to the  
negative control group. The main lesions were recorded in  
liver, spleen, and intestine. Regarding to the experimental  
infection by using different Salmonella species including  
S. Bargny, S. Tshingwe, S. Uganda, S. Kentucky, and S.  
Enteritidis, the histopathological finding are summarized  
and presented in table 10 and from this table, it is clear  
that the degenerative effect and necrotic effect in liver,  
also depletion and macrophage infiltration were more  
remarkable in S. Tshingwe (Figure 1) than S. Bargny  
(Figure 2) and S. Uganda (Figure 3) in the first week post-  
infection, also the degenerative effect in the liver in  
second week post-infection was clearer in S. Bargny  
(Figure 4) than S. Uganda, S. Kentucky (Figure 5) and S.  
Enteritidis, macrophage infiltration in spleen is clear in S.  
Bargny and S. Uganda than S. Kentucky and S. Enteritidis  
(Figure 6).  
Table 1. Numbers and percentage of isolated salmonellae  
from different samples in integrated duck-fish farming  
Salmonella  
Types of  
samples  
Total number of  
samples  
Number  
of isolates  
%
2.9  
8
Litter samples  
Water  
samples  
69  
50  
2
4
Liver a  
Fecal swabs b  
60  
200 (pooled sample)  
379  
5
8
8.3  
4
Total  
19  
5
from scarifying ducks and duckling b 3 pooled sample (2-3 individual  
a
samples) were taken from each farm  
Clinical signs, postmortem findings and mortality  
rate during experimental infection with chosen  
Salmonella isolates  
Clinical signs were recorded as mentioned in table 5,  
from this table it is clear that the clinical signs were  
detected in all infected groups 24-48 hours PI in the form  
of extreme thirst, profuse diarrhea, huddling together as  
chilled, ruffled feather in some of them, lameness  
appeared in S.Bargny. Staggering gait appeared in  
S.Tshingwe 24hrs PI and in S.Enteritidis 72 hrs. PI. This  
was followed by retraction of the head towards the chest,  
later by tremors, retraction of the neck backward, paddling  
movement, coma, and death. Gross lesions of dead and/or  
sacrificed birds from the five infected groups were  
recorded and mentioned in table 5, from this table it is  
clear that the gross lesions revealed severe congestion of  
all internal organs, enlargement of the spleen,  
enlargement, and lobulation of the kidney, distention of  
the ureters with urates and typhlitis with frothy content. S.  
Bargny and, S.Enteritidis groups appeared to have necrotic  
foci on liver. Also, liver appeared very pale in third week  
PI in each of S. Uganda, S. Kentucky, and S.Enteritidis  
Also, hyperplasia in lining epithelium of examined  
intestine was higher in S. Bargny followed by S.  
Enteritidis as compared with each of S. Uganda and S.  
Kentucky while the histopathological changes in the third  
week post-infection were less remarkable than the  
previous weeks. Hyperplasia of the lining epithelium of  
examined intestine was more remarkable in cases infected  
with S. Bargny and S. Uganda compared to each of S.  
Kentucky and S. Enteritidis while enteritis was not  
detected in cases infected with S. Uganda and S.  
Kentucky.  
Also, ducks infected with S. Kentucky from two  
weeks post-infection showed hepatic vacuolation and a  
mild degree of histiocytic proliferation in spleen (Figure  
7).  
186  
J. World Poult. Res., 10(2S): 184-194, 2020  
Table 2. Biochemical characters of isolated Salmonella from different samples in integrated duck-fish farming  
TSI  
Items  
Motility  
Indole  
M.R  
V.P  
urea  
H2S  
gas  
Butt  
slant  
Salmonella isolates  
+
-
+
-
+
+
Y
R
-
M.R: methyl red. V.P: Voges-Proskauer. TSI: triple sugar iron. H2S: hydrogen sulfide. The samples used were poultry litter samples and water samples from  
fish farms as well as cloacal swabs and liver samples from ducks.  
Table 3. Serotypes of isolated Salmonella from different samples in integrated duck-fish farming  
Salmonella  
incidence  
Types of samples  
Number of samples  
Number of isolates  
Identified serotypes  
S. Gueuletapee  
S. Tshiongwe  
Water samples  
69  
2
2.89%  
S. Bargny  
S. Cuckmere  
S. Belgdam  
S. Kentucky  
Litter samples  
Liver samples a  
50  
60  
4
5
8%  
S. Enteritidis  
S. Brikama  
S. Amesterdam  
S. Kentucky  
S. Kulsrivier  
8.3%  
S. Atakpame  
S. Kentucky (2 isolates)  
S. Oxford  
200  
Cloacal swab samples b  
8
4%  
S. Enteritidis  
S. Ferruch  
Pooled samples  
S. Uganda  
S. Bargny  
a from scarifying ducks and duckling b 3 pooled sample (2-3 individual samples) were taken from each farm  
Table 4. Antigenic profile of isolated Salmonella from different samples in integrated duck-fish farming  
Antigenic structure profile  
H antigen  
Serotype  
O antigen  
Phase I  
Phase II  
S. Ferruch  
8
8,20  
e,h  
1
1,5  
S. Bargny  
1,5  
S. Brikama  
S. Tshiongwe  
S. Amesterdam  
S. Uganda  
8,20  
r,i  
l,w  
6,8  
e,h  
e,n,z15  
3,10,(15),(15,34):  
3,10,(15)  
9,46  
g,m,s  
1,Z13  
g,m,q  
-
15  
-
S. Belgdam  
S. Atakpame  
S. Gueuletapee  
S. Oxford  
8,20  
1,9,12  
e,h  
g,m,s  
A
1,7  
-
3,10,(15),(15,34)  
3,10  
1,7  
1,2  
e,n,x  
-
S. Cuckmere  
S. Kulsrivier  
S. Enterididis  
S. Kentucky  
I
1,9,12  
g,m,s,t  
g,m  
I
1,9,12  
8,20  
Z6  
O antigen: somatic antigen. H antigen: flagellar antigen. The samples used were poultry litter samples and water samples from fish farms as well as cloacal  
swabs and liver samples from ducks.  
187  
 
El-nabarawy et al., 2020  
Table 5. Clinical signs and postmortem lesions in experimentally infected 7-day-old ducks with different Salmonella serovars.  
Symptoms  
Experimentally infected groups with different Salmonella serovars  
Control  
Group 1  
Group 2  
Group 3  
Group 4  
Group 5  
(S. Bargny)  
(S. Tshingwe)  
(S. Uganda)  
(S. Kentucky)  
(S. Enteritidis)  
Diarrhea  
+ve  
+ve  
+ve  
-ve  
-ve  
+ve  
-ve  
-ve  
+ve  
+ve  
+ve  
+ve  
+ve  
+ve  
-ve  
-ve  
+ve  
+ve  
-ve  
+ve  
+ve  
+ve  
+ve  
-ve  
+ve  
+ve  
+ve  
+ve  
+ve  
+ve  
-ve  
-ve  
-ve  
-ve  
-ve  
-ve  
-ve  
-ve  
-ve  
Huddling  
Weakness  
Ruffled feathers  
Nervous manifestation  
Increase thirst  
Reduced feed intake  
Lameness  
-ve  
-ve  
-ve  
+ve  
+ve  
+ve  
+ve  
+ve  
+ve  
Post mortem lesions  
Group 1  
Group 2  
Group 3  
Group 4  
Group 5  
Control  
Congested liver  
+ve  
+ve  
-ve  
-ve  
+ve  
-ve  
+ve  
+ve  
+ve  
+ve  
-ve  
+ve  
+ve  
-ve  
+ve  
+ve  
-ve  
-ve  
-ve  
+ve  
+ve  
-ve  
+ve  
+ve  
+ve  
+ve  
-ve  
-ve  
-ve  
-ve  
-ve  
-ve  
Congested spleen  
Enlarged kidney  
Ureter filled with urates  
+ve  
-ve  
+ve  
Necrosis of liver  
Pale liver (3rd week)  
+ve: positive. -ve: negative.  
-ve  
Table 6. Mortality pattern and mortality rate in experimentally infected 7-day-old ducks with different Salmonella serovars.  
Time 1st week  
2nd week  
3rd week  
Mortality rate  
1st day  
2nd day  
3rd day  
4th day  
Groups  
Group 1 (S.Bargny)  
Group 2 (S.Tshingwe)  
Group 3 (S.Uganda)  
1
1
-
-
1
3
1
-
2(sacrified)  
-
2(sacrified)  
-
28.6%  
100%  
42.9%  
2
1
1
1
2(sacrified)  
2(sacrified)  
Group 4 (S.Kentucky)  
Group 5 (S.Enteritidis)  
Control group  
-
-
-
-
1
-
1
-
1
1
-
2(sacrified)  
2(sacrified)  
2(sacrified)  
2(sacrified)  
2(sacrified)  
2(sacrified)  
28.6%  
28.6%  
0%  
-
Table 7. Duration of fecal Salmonella shedding in experimentally infected ducks with different Salmonella serovars  
Group 1  
(S. Bargny)  
total  
Group 2  
(S. Tshingwe)  
total  
Group 3  
(S. Uganda)  
total  
Group 4  
(S. Kentucky)  
total  
Group 5  
(S. Enteritidis)  
total  
Control  
Shedding  
+ve  
4
%
57  
+ve  
2
%
+ve  
3
%
42.9  
28.6  
33.3  
100  
25  
+ve  
1
%
+ve  
%
+ve  
0
birds  
birds  
birds  
birds  
birds  
First day  
7
6
7
28.6  
66.6  
25  
7
7
7
14.3  
42.9  
28.6  
100  
40  
1
1
3
1
1
1
8
7
14.3  
14.3  
50  
Second day  
Third day  
Fourth day *  
2
33  
4
6
4
2
3
7
7
7
6
0
1
6
16.6  
1
2
6
2
0
-
-
1
1
100  
-
1
1
1
1
1
100  
20  
0
Second  
week  
2
5
40  
-
-
1
4
2
5
5
0
Third week  
3
3
100  
44.4  
-
-
-
1
2
50  
2
3
66.6  
36.6  
3
33.3  
27.5  
0
Total  
12  
27  
8
18  
44.4  
10  
27  
37.4  
11  
30  
29  
0
*cloacal swabs collected in 4th day post-infection only from dead ducks. +ve: positive.  
-ve: negative  
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J. World Poult. Res., 10(2S): 184-194, 2020  
Table 8. Recovery of Salmonella from different organs of freshly dead and /or sacrificed ducks after oral experimental  
infection with different Salmonella serovars  
Group 1  
(S. Bargny)  
Group 2  
(S. Tshingwe)  
Group 3  
(S. Uganda)  
Group 4  
(S. Kentucky)  
Group 5  
(S. Enteritidis)  
Control  
Total  
Organ  
No.  
%
No.  
%
No.  
%
No.  
%
No.  
%
No.  
No.  
%
Liver  
3/6  
3/6  
2/6  
50  
3/7  
42.9  
2/7  
28.6  
2/6  
33  
2/6  
33  
-
12/32  
37.5  
Spleen  
50  
4/7  
2/7  
2/7  
11  
57.1  
28.6  
28.6  
39.3  
4/7  
3/7  
2/7  
11  
57.1  
28.6  
28.6  
39.3  
3/6  
1/6  
1/6  
7
50  
4/6  
2/6  
1/6  
9
66.7  
33  
-
-
-
-
18/32  
10/32  
8/32  
56.2  
31.2  
25  
Gall bladder  
33.3  
33.3  
41.7  
16.6  
16.6  
29.2  
Heart blood  
2/6  
10  
16.6  
37.5  
Total  
No.: Number  
Table 9. Performance analysis of seven-day-old duckling under Salmonella infection  
Groups  
Group 1  
(S. Bargny)  
Group 2  
(S. Tshingwe)  
Group 3  
(S. Uganda)  
Group 4  
(S. Kentucky)  
Group 5  
(S. Enteritidis)  
Control  
173±8.7  
415±13.1  
100  
Parameters  
Initial body weight (g; M±SE)  
170±5.3  
336±8.7***  
81  
172±5.7  
172±5.5  
365.7±8.3***  
88  
170±6.2  
359±17***  
86.5  
171.71±6.8  
Final body weight (g; M±SE)  
0
0
0
332±6.6***  
80  
Relative average final body weight (%)  
Body weight gain (g; M±SE)  
158±5.7***  
192±3.9***  
175.6± 2.48***  
158.2±3.52***  
230±2.26***  
Relative average body weight gain (%)  
Feed intake (g)  
68.6  
846  
87  
0
0
0
79.8  
986  
78.1  
941  
66.5  
829  
100  
972  
100  
Relative average feed intake (%)  
101.4  
96.8  
85.5  
Feed conversion ratio  
5.1  
0
0
5.11  
4.98  
5.15  
4.02  
100  
Relative average feed conversion ratio (%)  
126.9  
127.1  
123.9  
128.1  
*** Significant difference (p<0.001) compared to control; group. M ± SE: mean ± standard error  
Table 10. Semi-quantitative assessment of the histopathological score in experimentally infected ducks with different  
Salmonella serovars  
Liver  
Spleen  
Intestine  
Sampling time  
(week post-  
infection )  
Isolates  
Lymphoid  
depletion  
Macrophage  
infiltration  
Hyperplasia of the  
lining epithelium  
Degeneration  
Necrosis  
Enteritis  
S. Bargny  
S.Tshingwe  
S.Uganda  
1
1
1
2
2
2
2
3
3
3
3
++++  
++++  
+++  
+++  
++  
+++  
+++  
++  
+++  
+++  
+++  
+++  
++  
++++  
++++  
++  
++  
S.Bargny  
++  
++  
++  
++++  
++  
++  
+++  
++  
++  
+
S.Uganda  
++  
++  
+
S.Kentucky  
S.Enteritidis  
S.Bargny  
++  
+
+
+
++  
+
+
++  
+
++  
+
+
++  
+
S.Uganda  
++  
+
+
++  
+
S.Kentucky  
S.Enteritidis  
++  
Not detected  
Not detected  
Not detected  
Not detected  
++  
Not detected  
Not detected  
++  
++  
+
+ mild, ++ moderate ,+++ severe focal and ++++ severe diffuse lesions  
189  
 
El-nabarawy et al., 2020  
Figure 1. Diffuse necrosis of the lymphoid tissue mostly  
Figure 4. vacuolation of hepatocytes (arrow A) associated  
with bile duct lining epithelium hyperplasia (arrow B) in  
liver of ducklings infected with Salmonella Bargny and  
sacrificed 2 weeks post-infection.  
of liquefactive type (arrow A) in spleen of ducklings  
infected with Salmonella Tshingwe and sacrificed 7 days  
post-infection.  
Figure 5. Mononuclear cells infiltration consisted mainly of  
lymphocytes and macrophages (arrows) and diffuse  
vacuolation of hepatocytes in liver of ducklings infected with  
Salmonella Kentucky and sacrificed 2 weeks post-infection.  
Figure 2. Large necrotic foci (arrow A) in liver of  
ducklings infected with Salmonella Bargny and sacrificed  
7 days post-infection.  
Figure 3. Lymphoid depletion associated with increase the  
inflammatory cell infiltration within the splenic  
parenchyma (arrow A) in spleen of ducklings infected  
with Salmonella Uganda and sacrificed 7 days post-  
infectionn  
Figure 6. Mild degree of lymphoid depletion (arrow A)  
and minimal macrophages infiltration (arrow B) in spleen  
of ducklings infected with Salmonella Enteritidis and  
sacrificed 2 weeks post-infection.  
190  
 
J. World Poult. Res., 10(2S): 184-194, 2020  
by Mondal et al. (2008) who examined 65 fecal swabs  
from ducks and reported Salmonella with a rate 13.07 %  
but it is higher than that reported by Hegazy (1991) who  
isolate Salmonella from cloacal swabs of ducks and  
duckling with incidence 0.98% and 0.72% respectively.  
Salmonellae have the ability to multiply and survive  
in internal organs particularly spleen and liver because  
these organs can provide places where bacterial  
multiplication can arise without interruption by host  
defense mechanism (Gast, 2003). Liver showed  
Salmonella isolation with an incidence of 8.3%. Many  
authors succeeded to isolate Salmonella from liver with a  
more or less identical incidence as Badr et al. (2015)  
reported four Salmonella isolates from the liver of ducks  
with a percentage of 6.45%. Also, this incidence is nearly  
similar to that isolated by Selvaraj et al. (2010) from  
poultry in India with incidence (6.25%). However, it was  
lower than that reported in Egypt by Abd-Elghany et al.  
(2015) who reported Salmonella from the chicken liver  
with an incidence of 32%.  
In this study, a total of 13 Salmonella isolates were  
obtained from duck farms integrated with fish farms (200  
cloacal swabs and 60 liver samples) with incidence (5%)  
but this percent is lower than that reported by Lebdah et  
al., (2017) from ducks in Dakahlia and Damietta  
Governorates in Egypt with a rate (11.7%), (Mahmoud  
and Moussa, 2000) reported 25 positive samples for  
Salmonella out of 125 samples from 10 duck flocks in  
North Sinai with 20% rate.  
Salmonella Uganda isolated from ducks in this study  
with a rate of 7.7% and this may be the first report of S.  
Uganda isolation from ducks in Egypt according to the  
available literature. This serovar was predominantly  
isolated from pigs and it was responsible for 4 pork-  
associated outbreaks in humans between 1998 and 2008 in  
In this study, the mortality ranged from 28.6% in S.  
Bargny, S. Enteritidis, and S. Kentucky and increased to  
42.9% in S.Uganda and reached up to 100% in S.  
Tshingwe. there is no report about the mortality rate of  
some of these serotypes according to the available  
literature, however, Osman et al., (2010) reported the  
mortality of S.Enteritidis in chicken with a rate 88% also  
they reported the mortality in case of S. Kentucky with a  
rate 40%. Hegazy (1991) reported mortalities from S.  
Enteritidis from ducklings with a rate of 10% while no  
mortalities were reported in S. Tshingwe infected group.  
In agreement with another investigator, Copper et al.,  
(1992) and Barrow (2000) the postmortem lesions in dead  
and/or sacrificed ducks generally included congestion of  
Figure 7. Perivascular histiocytic and macrophages  
infiltration (arrow A) in spleen of ducklings infected with  
Salmonella Kentucky and sacrificed 3 weeks post-  
infection.  
DISCUSSION  
Transmission of Salmonella species to waterfowls can be  
mediated by contaminated feeds, water, and litter (Gast  
2003; Grigar et al., 2017). In the present work, Salmonella  
was isolated from litter with a rate of 8%, this rate appears  
to be higher than that previously reported in Egypt by  
Dahshan et al. (2015) who reported a rate of 4%.  
However, Rusul et al. (1996) reported that the isolation  
rate of Salmonella from broiler litter was 20% also  
Abunna et al. (2016) reported Salmonella from poultry  
litter with a rate of 40%. The recorded high rates of  
Salmonella in poultry litter in this study may be due to the  
different epidemiological picture of Salmonella infection  
and its shedding in poultry farms in governorates that  
integrated with fish farms breeding and waterfowls  
production 8% rather than other governorates with less  
integrated fish production and this indicates the role of  
integrated waterfowls and fish farms of the incidence and  
distribution of Salmonella infection and its ecological  
impact, also the unhygienic measurement in small-scale  
poultry farms in Kafr El-Sheikh Governorate and it poses  
a critical point for Salmonella transmission to fish farms in  
the integrated systems because the large scale farms are  
under veterinary supervision.  
Salmonella spp. can be reached to aqua-system by  
fecal contamination and it has been reported in freshwater  
fish culture ponds in many countries and also may be  
present naturally in tropical aquatic environments  
In the present study, salmonellae were isolated from  
ducks cloacal swabs with a rate of 4% (8 out of 200  
pooled samples). This percent is lower than that reported  
191  
El-nabarawy et al., 2020  
internal organs, enlargement of spleen, typhlitis and  
Authors’ contribution  
distention of ureter with urates.  
Anwaar Mettwally El-Nabarawy contributed in  
planning, interpretation, and revision of the research,  
Mohamed Abdel Salaam Shakal design the idea for the  
research, Abdel-Haleem Mohamed Hegazy contributed in  
following up adoption of methodology and Mohamed  
Mohamed Ismail Batikh contributed through performing  
technical works including sampling, isolation and  
identification, experimental infection, collecting data and  
data analysis. All authors approved the final manuscript.  
Experimental Salmonella infection resulted in  
changes in feed consumption, body weight, and feed  
conversion. The relative average feed consumption for the  
infected groups was 13%, -1.4%, 3.2% and 14.5% for S.  
Bargny, S. Uganda, S. Kentucky, and S. Enteritidis,  
respectively with missing the data belonging to  
S.Tshingwe because the mortality in this group reached to  
100% in the first 48 hr. relative average body weight was  
also affected and showed a reduction ranged from 20.2%  
to 33.5% among the infected groups at the end of the  
experiment. These data are in a general agreement with  
The histopathological picture was in general  
agreement with that described by several investigators for  
paratyphoid infection in ducks as El-Sawy, (1976) and  
al., (2004). However, it is interesting to note that liver  
degeneration and necrosis with lymphoid depletion and  
macrophage infiltration were more severe in case of S.  
Tshingwe and this may explain the high mortalities that  
reached to 100% among this group.  
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