Skip to content

Advertisement

  • Research article
  • Open Access

Non-typhoidal Salmonella serovars in poultry farms in central Ethiopia: prevalence and antimicrobial resistance

BMC Veterinary Research201814:217

https://doi.org/10.1186/s12917-018-1539-4

  • Received: 15 February 2018
  • Accepted: 21 June 2018
  • Published:

Abstract

Background

Poultry is one of the common sources of non-typhoidal Salmonella and poultry products are the major sources of human infection with non-typhoidal Salmonella. In spite of flourishing poultry industry in the country, data on prevalence and antimicrobial susceptibility of non-typhoidal Salmonella serovars at farm level is not available in Ethiopia. This study investigated prevalence, serotype distribution and antimicrobial resistance of non-typhoidal Salmonella in poultry farms in Addis Ababa and its surrounding districts.

Results

A total of 549 fresh pool of fecal droppings (n = 3 each) were collected from 48 poultry farms and cultured for Salmonella using standard laboratory technique and serotyped using slide agglutination technique. Susceptibility of Salmonella isolates to18 antimicrobials was tested according to CLSI guideline using Kirby-Bauer disk diffusion assay. Salmonella was recovered in 7 (14.6%) of the farms and 26 (4.7%) of the samples. Salmonella was more common in poultry farms with larger flock size than in the smaller ones and in Ada’a district as compared to other districts. All isolates were obtained from farms containing layers. Two out of 6 (33.3%) farms that kept birds in cage were positive for Salmonella while only 5 (11.9%) of the 42 farms who used floor system were positive. Oxytetracycline was used widely in 40 (83.3%) of the farms, followed by amoxicillin 14 (29.2%) and sulfonamides 11 (22.9%). Salmonella Saintpaul was the dominant serotype detected accounting for 20 (76.9%) of all isolates. Other serovars, such as S. Typhimurium3 (11.5%), S. Kentucky 2 (7.7%) and S. Haifa 1 (3.8%) were also detected. Of all the Salmonella isolates tested, 24 (92.3%) were intermediately or fully resistant to sulfisoxazole and streptomycin, 12 (46.2%) to cephalothin, while 11 (42.3%) were resistant to ampicillin, amoxicillin+clavulanic acid, kanamycin and chloramphenicol. Multidrug resistance (MDR) to several drugs was common in S. Kentucky and S. Saintpaul.

Conclusion

Despite low prevalence of Salmonella in poultry farms in the study area, circulation of MDR strains in some farms warrant special biosecurity measures to hinder dissemination of these pathogens to other farms and the public. Moreover, awareness creation on prudent use of antimicrobials is recommended.

Keywords

  • Poultry
  • Non-typhoidal Salmonella
  • Antimicrobial resistance
  • Prevalence
  • Ethiopia

Background

Salmonella is one of the major causes of food-borne diseases worldwide [1]. Poultry and other food animals are considered the common reservoirs of Salmonella enterica and undercooked poultry products are the major sources of human infection with non-typhoidal Salmonella [2, 3]. Several host unrestricted S. enterica serovars frequently isolated from poultry without showing any clinical signs usually infect a wider range of hosts and cause disease in humans as well [4].

It has been shown that some of the most commonly detected serovars in chickens in a given geographic area are also among the top serovars associated with human infections indicating the role of Salmonella colonization of poultry farms to public health [5]. Knowledge on distribution of Salmonella serovars in food animals and humans is useful to understand the trends of Salmonella epidemiology and to identify serovars that cluster over time and space. Temporal and spatial variation in rate and distribution of Salmonella serovars in poultry industry has been reported [2, 6].

Developed countries conduct routine surveillance of Salmonella in poultry farms to understand the level of colonization by Salmonella, serovars involved and drug resistance profile with the aim of designing ways of reducing public health salmonellosis of poultry origin [7, 8]. However, in developing countries like Ethiopia, little effort is made to monitor Salmonella in poultry farms and information on prevalence and serotype distribution as well as phenotypic and genotypic relatedness of Salmonella isolated from poultry and humans is not well documented. Local knowledge on prevalence of Salmonella, serotype distribution and associated risk factors is important to implement appropriate control strategy to reduce wider dissemination of important zoonotic serovars [2].

There is little available literature on farm level prevalence and serotype distribution of non-typhoidal Salmonella in poultry farms in Ethiopia. Previous studies conducted on retail raw chicken products reported 17.9% prevalence of Salmonella, the dominant serovars being S. Braenderup (31.5%), S. Anatum (25.9%), S. Saintpaul (14.8%) and S. Uganda (11.1%) [9]. Another study also reported that 14% of chicken carcass from supermarkets in Addis Ababa were positive for Salmonella. S. Braenderup (41.4%), S. Hadar (20.7%), S. Newprt (13.8%) and S. Typhimurium (10.3%) were the dominant serovars detected in poultry products in Addis Ababa [10]. However, source of Salmonella contamination in these poultry products could be either from farm or due to cross contamination during slaughter, transportation or storage. Recent study in southern Ethiopia showed that 16.7% of samples from poultry and the environment of three poultry farms were positive for Salmonella although this study did not show whether Salmonella isolates were host specific Salmonella serovars or host unrestricted non-typhoidal Salmonella serovars [11].

Majority of the Salmonella isolates from poultry products and poultry farms in the previous studies were found to be resistant to several antimicrobials. Information on farm level prevalence and antimicrobial susceptibility status of isolates can explain the level of public health risk associated with poultry products. The aim of this study was therefore to determine the prevalence, serotype distribution and antimicrobial resistance of salmonella in poultry farms in central Ethiopia. The type of antimicrobials and disinfectants commonly employed in poultry farms were also assessed.

Methods

Study design, study area and study animals

A cross-sectional study was conducted in Addis Ababa and 3 districts of Oromia region located at the outskirt of Addis Ababa from July 2013–January 2014. A total of 549 pooled fresh fecal droppings (from 3 chicken each) were collected in 48 farms (Ada’a district n = 33, Addis Ababa n = 6, Sebeta n = 6, Barake n = 3). Inclusion of farms in the sampling was based on representation of the area under study, willingness of the owners, availability of poultry farms in the study area, and the flock having a minimum of 50 birds. Most of the poultry farms investigated in the current study were those from Ada’a district due to large number of poultry farms in this district.

Data and sample collection

Information such as type of poultry farm, whether it is broiler or layer, flock size, birds housing system, age of birds, purpose and types of antimicrobials and disinfectants commonly used in the farm during the last 6 months were recorded using a purposively designed questionnaire. Collection of data was performed at the time of fecal sample collection from each farm. Pooled fresh fecal droppings(from 3 chickens) were collected using clean disposable gloves in to sterile zippered plastic bags which were transported to microbiology laboratory of Aklilu Lemma Institute of Pathobiology, Addis Ababa University in an ice box within 3–4 h of collection.

Salmonella isolation, identification, serotyping and phage typing

Salmonella isolation and identification was carried out using conventional methods [12, 13]. Briefly, fresh fecal droppings from three chicken was thoroughly mixed of which 10 g of feces was suspended in 90 ml of buffered peptone water (BPW) (Becton Dickinson, Sparks, MD) and incubated overnight at 37 °C. Enrichment, culturing on selective media, and biochemical analysis of presumptive Salmonella colonies was conducted as shown previously [14]. Genus specific PCR was used to confirm isolates suspected to be Salmonella by biochemical tests [15]. Salmonella Typhimurium (ATCC 14028) was used as a positive control during biochemical analysis and PCR. Confirmed Salmonella isolates were stored at − 80 °C in 20% glycerol till further investigation.

Serotyping and phage typing of Salmonella isolates was conducted at the World Organization for Animal Health (OIÉ) Reference Laboratory for salmonellosis, Public Health Agency of Canada’s National Microbiology at Guelph. Determination of serovars was conducted using serum agglutination technique as shown previously [16, 17], based on identification of somatic (O) antigens [18] and flagellar (H) antigens [19].

Antimicrobial susceptibility testing

Isolates were investigated for susceptibility to 18 antimicrobials using the Kirby-Bauer disk diffusion method according to Clinical and Laboratory Standards Institute guidelines [20]. Antimicrobials used in the current study were amikacin (30 μg), amoxicillin + clavulanic acid (20/10 μg), ampicillin (10 μg), cefoxitin (30 μg), ceftriaxone (30 μg), cephalothin (30 μg), chloramphenicol (30 μg), ciprofloxacin (5 μg), gentamicin (10 μg), kanamycin (30 μg), nalidixic acid (30 μg), neomycin (30 μg), nitrofurantoin (100 μg), streptomycin (10 μg), sulfisoxazole (1000 μg), sulfamethoxazole + trimethoprim (23.75/1.25 μg), trimethoprim (5 μg) and tetracycline (30 μg). All of them were from Sensi-Discs, Becton, Dickinson and Company, Loveton, USA. The interpretation cut off points for susceptibility status of isolates was based on the CLSI guidelines [20]. For the purpose of analysis, all readings classified as intermediate were considered as resistant unless indicated. E. coli ATCC 25922 was used as a quality control organism.

Statistical analysis

Sample level prevalence of Salmonella was calculated as percentage of Salmonella culture positive fecal samples among total number of samples examined. Farm level prevalence was calculated as the percentage of farms with one or more Salmonella culture positive pooled fecal sample among the total farms sampled. Association of Salmonella detection with various factors was tested using exact test and p-value < 0.05 was considered significant.

Results

Farm level Salmonella occurence with respect to various factors

Salmonella was isolated from 14.6% (7/48) of poultry farms with individual sample level prevalence of 4.7% (Table 1). Salmonella was more common in poultry farms with larger flock size and in age group of 2–6 months (Table 2). Majority of the farms studied contained layers or young pullets grown for egg production (n = 43, 89.6%); whereas only (n = 5; 11.4%) were keeping broilers. Salmonella was not detected from the broiler farms. Salmonella isolation was also more common in farms of the Ada’a district as compared to other districts. Majority of the farms (n = 42; 87.5%) keep their birds on floor system and 12.5% (6/48) use cage system. Out of the farms that use cage system 33.3% (2/6) were positive for Salmonella whereas 11.9% (5/42) of farms that use floor system were found positive for Salmonella.
Table 1

Prevalence of Salmonella in poultry farms in Addis Ababa and surrounding districts

 

No. of farms

Average no. of birds /farm

No. of samplesa

No. positive samples

% positive samples

(%) positive farms

Ada’a

33

4638

464

25

5.4

18.2

Addis Ababa

6

1075

45

1

2.2

16.7

Barake

3

395

18

0

0

0

Sebeta

6

627

22

0

0

0

Total

48

1684

549

26

4.7

14.6

aSamples were pool of fecal droppings from 3 chicken

Table 2

Occurrence of Salmonella in poultry farms stratified by selected factors

Selected Factors

No. of farms

No. of Salmonella positive farms

% of farms positive for Salmonella

p-value*

Commodity type

 Layers

43

7

16.3

1.000

 Broilers

5

0

0

 

Use of disinfectants

 Yes

26

6

23.1

0.106

 No

22

1

4.5

 

Age of birds in months

  < 2

8

0

0

0.608

 2–6

17

4

24

 

 7–12

13

2

15.4

 

  > 12

10

1

10

 

Flock size

  < 1000(Small)

22

2

9.1

0.648

 1000–5000(Medium)

17

3

17.7

 

  > 5000(Large)

9

2

22.2

 

Poultry housing system

 Floor

42

5

11.9

0.206

 Cage

6

2

33.3

 

*Exact test was used to obtain p-value

Antimicrobials used in poultry farms

Among the common antimicrobials, oxytetracycline was used widely in 40 (83.3%) of the farms, followed by amoxicillin (29.2%) and sulfonamides (22.9%). Other antimicrobials such as fluoroquinolones (enrofloxacin and ciprofloxacin), and florfenicol were also used in 11 (22.9%) and 7 (14.6%) of the farms respectively, whereas 6(12.5%) of the farms reported that they did not use any antimicrobials during last 6 months. None of the farms reported use of antimicrobials as feed additive. All of the farms use antimicrobials for therapeutic or prophylactic purposes when there is one or more sick birds in the flock. Interestingly, in one of the poultry farms in Adaa district, the use of human preparation of ciprofloxacin tablet was observed. Salmonella was recovered more frequently in farms which use only amoxicillin, sulfadimidine and oxytetracycline than those farms which use fluoroquinolones and florfenicol. Recent use of antimicrobials and occurrence of Salmonella in farms is shown in Table 3. All samples from six farms with no history of use of antimicrobials were also not culture positive for Salmonella. Twenty-three (47.9%) of the farms reported use of sodium hypochlorite disinfectant as foot bath, for cleaning poultry houses before introduction of new stock and to clean feeding utensils, while 4(8.3%) of the farms used copper sulfate. The remaining 21(43.8%) of the poultry farms were not using any disinfectant.
Table 3

Recent use of antimicrobials and occurrence of Salmonella in poultry farms

Type of Antimicrobials used during the last 6 months

No. of farms

No. of Salmonella positive farms

% of farms positive for Salmonella

Amoxicillin only

2

0

0

Oxytetracyline only

18

4

22.2

Oxytetracycline + ciprofloxacin

3

0

0

Oxytetracycline + florfenicol + enrofloxacin

4

0

0

Oxytetracycline + sulfonamides

3

1

33.3

Oxytetracycline + amoxicillin

4

1

25

Oxytetracycline + sulfonamides + amoxicillin

8

1

12.5

Did not use antimicrobial agent

6

0

0

Salmonella serotype distribution and antimicrobial susceptibility

Salmonella Saintpaul was the dominant serotype detected in poultry farms accounting for 20 (76.9%) of all isolates. Other serotypes, such as S. Typhimurium (n = 3), S. Kentucky (n = 2) and S. Haifa (n = 1) were also detected. Rate of resistance to antimicrobials tested and resistance patterns of the isolates are shown in Tables 4 and 5 respectively. Of all the Salmonella isolates tested, (n = 24, 92.3%) were resistant to sulfisoxazole and streptomycin, (n = 12, 46.2%) of the isolates were resistant to cephalothin, while (n = 11, 42.3%) were resistant to ampicillin, amoxicillin + clavulanic acid, kanamycin and chloramphenicol (Table 4).
Table 4

Salmonella serovar distribution and rate of resistance to antimicrobial agents

Antimicrobial agents

Salmonella serovars and resistance ratea

Total No. (%) resistant

S. Saintpaul

(n = 20)

S. Typhimurium

(n = 3)

S. Kentucky

(n = 2)

S. Haifa

(n = 1)

No. resistant (%)

No. resistant (%)

No. resistant (%)

No. resistant (%)

Ampicillin

9 (45)

0

2 (100)

0

11 (42.3)

Amoxicillin+clavulanic acid

9 (45)

0

2 (100)

0

11 (42.3)

Chloramphenicol

10 (50)

0

1 (50)

0

11 (42.3)

Cephlothin

10 (50)

0

2 (100)

0

12 (46.2)

Ciprofloxacin

0

0

2 (100)

0

2 (7.7)

Cefoxitin

0

0

0

0

0

Gentamicin

0

0

2 (100)

0

2 (7.7)

Kanamycin

8 (40)

2 (66.7)

0

1 (100)

11 (42.3)

Sulfamethoxazole+trimethoprim

0

0

0

1 (100)

1 (3.9)

Trimethoprim

0

0

0

1 (100)

1 (3.9)

Tetracycline

4 (20)

1 (33.3)

2 (100)

1 (100)

8 (30.8)

Sulfisoxazole

18 (90)

3 (100)

2 (100)

1 (100)

24 (92.3)

Streptomycin

18 (90)

3 (100)

2 (100)

1 (100)

24 (92.3)

Nitrofurantoin

5 (25)

1 (33.3)

0

1 (100)

7 (26.7)

Nalidixic acid

2 (10)

0

2 (100)

1 (100)

5 (19

Neomycin

3 (15)

0

0

0

3 (11.5)

aIsolates with intermediate susceptibility were also considered resistant for this analysis

Table 5

Salmonella serotypes isolated from poultry farms and their antimicrobial resistance pattern

No.

Study site

Farm Code

Isolate code

Serotype

Resistance pattern

Intermediate

Resistant

1

Adaa

DZP-20

DP-213 T

Kentucky

C

Amp,Amc,Cf,Cip,Gm,Te,Su,S,Na

2

Adaa

DZP-20

DP-220 T

Kentucky

Amp,Amc,Cf,Cip,Gm,Te,Su,S,Na

3

Addis Ababa

AAP-08

AP-H2O

Haifa

K,S

Sxt,Tmp,Te,Su,Nitro,Na

4

Adaa

DZP-03

DP-23 T

Saintpaul

Su

5

Adaa

DZP-03

Dp-24 T

Saintpaul

Su,S

6

Adaa

DZP-03

Dp-25R

Saintpaul

SuS

7

Adaa

DZP-03

DP-26R

Saintpaul

Cip,Su,SNitro,N

8

Adaa

DZP-03

DP-27R

Saintpaul

Su,S

9

Adaa

DZP-11

DP-116 T

Typhimurium

K

Te,Su,S

10

Adaa

DZP-08

DP-70 T

Typhimurium

SuS

11

Adaa

DZP-08

DP-71 T

Typhimurium

K,Su,S,Nitro

12

Adaa

DZP-33

DP-107

Saintpaul

Amc,Cf,K,S

Amp,C,Te,Su

13

Adaa

DZP-33

DP-117

Saintpaul

Amc,Cf,K,S

Amp,C,Su

14

Adaa

DZP-33

DP-128

Saintpaul

-

 -

15

Adaa

DZP-33

DP-131

Saintpaul

K,S

16

Adaa

DZP-33

DP-110

Saintpaul

Amc,Cf,S

Amp,C,Te,Su

17

Adaa

DZP-33

DP-114

Saintpaul

SuS

 

18

Adaa

DZP-33

DP-126

Saintpaul

Cf,S

Amp,Amc,C,Su

19

Adaa

DZP-12

DP-313

Saintpaul

S,K

Amp,Amc,C,Cf,Te,Su

20

Adaa

DZP-12

DP-325

Saintpaul

Amc,Cf,Su,S,Nitro

Amp,Amc,C,Cf,Su,S,Nitro,Na

21

Adaa

DZP-12

DP-327

Saintpaul

K,S,Nitro

Su

22

Adaa

DZP-12

DP-328

Saintpaul

Amc,Cip,S,N

Amp,C,Cf,Te,Su

23

Adaa

DZP-12

DP-339

Saintpaul

K,Su,S

24

Adaa

DZP-12

DP-322

Saintpaul

Amc,Cf, Su,S,Nitro

Amp,Amc,C,Cf,Su,S,Nitro,Na

25

Adaa

DZP-12

DP-326

Saintpaul

Cf,S

Amp,Amc,C,Su

26

Adaa

DZP-12

DP-308

Saintpaul

Amc,Cip,K,Su,S,Na,N

Amp,C,Cf,Nitro

Amp ampicillin, Amc amoxicillin and clavulanic acid, Cf cephalothin, Cip ciprofloxacin, Gm gentamicin, K kanamycin, Tmp trimethoprim, Te tetracycline, Su sulfisoxazole, S streptomycin, Nitro nitrofurantoin, Na nalidixic acid, N neomycin, -sensitive

Overall, multidrug resistance was commonly detected in Salmonella isolates in the current study particularly in strains belonging to S. Saintpaul and the two S. Kentucky isolates. All S. Saintpaul strains in the current study were isolated from farms in Ada’a district. However, there was wide diversity in their antimicrobial susceptibility pattern even among isolates obtained from the same farm. Some of them were resistant to only few antimicrobials while others were MDR to several antimicrobials. The two S. Kentucky isolates were resistant to 9 of the 18 antimicrobials tested (Table 5).

Discussion

Colonization of poultry with Salmonella without detectable clinical signs at farm level followed by contamination of poultry products with subsequent access to human food chain has been considered as the major sources of human salmonellosis [21, 22]. Salmonella in healthy poultry is the main risk factor for possible outbreak of human salmonellosis and epidemiological studies have shown the huge contribution of contaminated poultry products to human salmonellosis [23, 24]. In fact, some countries have shown that successful control measures involving surveillance, improved biosecurity and vaccination targeting specific serovars in poultry can result in reduction of human salmonellosis cases [21, 24].

In the current study, 7(14.6%) of the 48 examined poultry farms were positive for Salmonella. This is very much low compared to studies conducted in Morocco and Nigeria where 76.7% and [25], 43.6% [26] of the poultry farms were contaminated by Salmonella, respectively. Sample level prevalence of Salmonella was also low in the current study (4.7%) compared to previous studies conducted elsewhere. For instance, Salmonella prevalence in fecal samples from conventional poultry farms in USA was reported to be 38.8% while it was 5.6% in organic farms [27]. Salmonella prevalence in conventional poultry is usually very high in different countries [2831]. The possible reason for low prevalence of Salmonella in the current study could be due to the fact that most of the poultry farms in the current study were small scale farms holding small number of birds unlike most of the large commercial poultry farms where they keep thousands of birds and the feeding and management activities associated with intensification allows easy dissemination of the pathogen within the farm. This finding is in agreement with previous report where large farms were significantly associated with high prevalence of Salmonella compared to medium and small farms [32].

Both farm level and pooled sample level prevalence of Salmonella was high in farms from Ada’a district compared to other areas, which could be due to larger number of poultry farms examined from this district compared to others as well as difference in agroecology. Ada’a district is highly concentrated with large number of poultry farms and is located in rift valley which is relatively warm region compared to Addis Ababa, Sebeta and Barake districts. The fact that most of the large poultry farms in the country including the parent stocks are located in Ada’a district and most of the farms from this area shared a single serotype, S. Saintpaul implies the possibility of transmission of Salmonella from farm to farm in this town. Salmonella Saintpaul is not frequently isolated from poultry in other previous studies elsewhere. Salmonella Kentucky was the dominant serovar in studies conducted in Nigeria [26] and Bangladesh [31] and S. Entertidis was dominant in Spain [33]; while S. Typhimurium was dominant in China [34]. Although there is no serotype data on Salmonella isolates from poultry at farm level in Ethiopia, previous study from poultry food items in Addis Ababa did not report S. Saintpaul [35]. As most of the farms obtain their day old chickens or pullets from a few parent stock farms located in this district, there is likelihood of contamination of poultry from source farms. In addition, S. Saintpaul was the major serotype detected in dairy farms in this study area which suggests possibility of transmission between dairy and poultry farms [14].

The high rate of resistance to sulfixazole and streptomycin (92.3%) is not concordant with the current rate of use of antimicrobials in farms investigated. However, previously, different sulfonamide drugs and streptomycin together with penicillin were the common antimicrobials frequently used in the country for treatment of various infectious diseases in veterinary medicine and recent studies showed that sulfonamides and streptomycin are the 2nd and 3rd most prescribed veterinary medications respectively in the study area next to oxytetracycline [36]. Similarly, high resistance rate to ampicillin and tetracycline could be due to long term use of these antimicrobials in veterinary medicine including poultry. Interestingly, the two S. Kentucky isolates resistant to several drugs including nalidixic acid and ciprofloxacin were isolated from one of a few farms which reported use of fluoroquinolones for therapeutic purposes in the farm suggesting possible contribution of use of these drugs in the farm for selection of these strains. Eleven (42.3%) of the isolates in the current study, most of which belonging to S. Saintpaul from farms in Ada’a district were resistant to chloramphenicol unlike previous study where all of the isolates obtained from food of animal origin including poultry products were fully susceptible to chloramphenicol [35]. Unlike previous study in south Ethiopia [11] where extremely high proportion of Salmonella isolates (97.8%) were resistant to second generation cephalosporin (cefoxitin), in this study, none of the isolates were resistant to this drug. This could be due to over use of betalactam drugs in the previous farms.

Conclusion

Despite low prevalence of Salmonella in poultry farms in the study area, circulation of MDR strains in some farms warrant special biosecurity measures to hinder dissemination of these pathogens to other farms and the public. Moreover, awareness creation on prudent use of antimicrobials is recommended.

Abbreviations

BPW: 

Buffered peptone water

MDR: 

Multi-drug resistance

RVB: 

Rappaport-vassiliadis broth

TTB: 

Tetrathionate broth

XLT-4: 

Xylose lysine tergitol 4

Declarations

Acknowledgments

The author would like to thank Mr. Haile Alemayehu and Mr. Nega Nigussie for their support during sample collection and laboratory analysis. Dr. Roger P. Johnson, Dr. Linda Cole, Shaun Kernaghan, Ketna Mistry, Ann Perets and Betty Wilkie of the Public Health Agency of Canada, National Microbiology Laboratory at Guelph are also acknowledged for serotyping of Salmonella isolates.

Funding

This study was supported by WHO Advisory Group on Integrated Surveillance of Antimicrobial Resistance. The funding agency was not involved in design of study, data collection, analysis of data and manuscript writing.

Availability of data and materials

All the data supporting the findings are presented in the manuscript.

Author’s contributions

TE was involved in conception of the study, laboratory work, data analysis and preparation of the manuscript.

Ethics approval and consent to participate

Study was approved by Institutional Review Board of Aklilu Lemma Institute of Pathobiology, Addis Ababa University and oral consent was obtained from the farm owners before sampling.

Consent for publication

Not applicable.

Competing interests

The author declares that he has no competing interests.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Authors’ Affiliations

(1)
Aklilu Lemma Institute of Pathobiology, Addis Ababa University, P.O. Box 1176, Addis Ababa, Ethiopia

References

  1. Zhao S, Datta AR, Ayers S, Friedman S, Walker RD, White DG. Antimicrobial-resistant Salmonella serovars isolated from imported foods. Int J Food Microbiol. 2003;84(1):87–92.View ArticlePubMedGoogle Scholar
  2. Foley SL, Nayak R, Hanning IB, Johnson TJ, Han J, Ricke SC. Population dynamics of Salmonella enterica serotypes in commercial egg and poultry production. Appl Environ Microbiol. 2011;77(13):4273–9.View ArticlePubMedPubMed CentralGoogle Scholar
  3. Braden CR. Salmonella enterica serotype Enteritidis and eggs: a national epidemic in the United States. Clin Infect Dis. 2006;43(4):512–7.View ArticlePubMedGoogle Scholar
  4. Gast RK. Serotype-specific and serotype-independent strategies for preharvest control of food-borne Salmonella in poultry. Avian Dis. 2007;51(4):817–28.View ArticlePubMedGoogle Scholar
  5. Foley SL, Lynne AM, Nayak R. Salmonella challenges: prevalence in swine and poultry and potential pathogenicity of such isolates. J Anim Sci. 2008;86(14 Suppl):E149–62.View ArticlePubMedGoogle Scholar
  6. Sivaramalingam T, McEwen SA, Pearl DL, Ojkic D, Guerin MT. A temporal study of Salmonella serovars from environmental samples from poultry breeder flocks in Ontario between 1998 and 2008. Can J Vet Res. 2013;77(1):1–11.PubMedPubMed CentralGoogle Scholar
  7. Wegener HC, Hald T, Lo Fo Wong D, Madsen M, Korsgaard H, Bager F, Gerner-Smidt P, Mølbak K. Salmonella control programs in Denmark. Emerg Infect Dis. 2003;9(7):774–80.View ArticlePubMedPubMed CentralGoogle Scholar
  8. Hendriksen RS, Vieira AR, Karlsmose S, Lo Fo Wong DM, Jensen AB, Wegener HC, Aarestrup FM. Global monitoring of Salmonella serovar distribution from the World Health Organization global foodborne infections network country data Bank: results of quality assured laboratories from 2001 to 2007. Foodborne Pathog Dis. 2011;8(8):887–900.View ArticlePubMedGoogle Scholar
  9. TibaiJuka B, B M, G H, J K. Occurrence of salmonellae in retail raw chicken products in Ethiopia. Berl Munch Tierarztl Wochenschr. 2003;116(1–2):55–8.PubMedGoogle Scholar
  10. Endrias Z, Poppe C. Antimicrobial resistance pattern of Salmonella serotypesisolated from food items and personnel in AddisAbaba, Ethiopia. Trop Anim Prod. 2009;41:241–9.View ArticleGoogle Scholar
  11. Abdi RD, Mengstie F, Beyi AF, Beyene T, Waktole H, Mammo B, Ayana D, Abunna F. Determination of the sources and antimicrobial resistance patterns of Salmonella isolated from the poultry industry in southern Ethiopia. BMC Infect Dis. 2017;17(1):352.View ArticlePubMedPubMed CentralGoogle Scholar
  12. Molla B, Sterman A, Mathews J, Artuso-Ponte V, Abley M, Farmer W, Rajala-Schultz P, Morrow WE, Gebreyes WA. Salmonella enterica in commercial swine feed and subsequent isolation of phenotypically and genotypically related strains from fecal samples. Appl Environ Microbiol. 2010;76(21):7188–93.View ArticlePubMedPubMed CentralGoogle Scholar
  13. WHO. Who Global Foodborne Infections Network Laboratory Protocol, Isolation of Salmonella spp From Food and Animal Feaces. 5th ed; 2010. http://antimicrobialresistance.dk/CustomerData/Files/Folders/6-pdf-protocols/63_18-05-isolation-of-salm-220610.pdf.
  14. Eguale T, Engidawork E, Gebreyes AW, Asrat D, Alemayehu H, Medhin G, Johnson RP, Gunn JS. Fecal prevalence, serotype distribution and antimicrobial resistance of salmonellae in dairy cattle in Central Ethiopia. BMC Microbiol. 2016;16(1):1–11.View ArticleGoogle Scholar
  15. Cohen ND, Neibergs HL, McGruder ED, Whitford HW, Behle RW, Ray PM, Hargis BM. Genus-specific detection of salmonellae using the polymerase chain reaction (PCR). J Vet Diagn Investig. 1993;5(3):368–71.View ArticleGoogle Scholar
  16. Grimont PAD, Weill FX. Antigenic Formulae of the Salmonella Serovars. 9th ed. Paris: Institut Pasteur; 2007.Google Scholar
  17. Issenhuth-Jeanjean S, Roggentin P, Mikoleit M, Guibourdenche M, de Pinna E, Nair S, Fields PI, Weill FX. Supplement 2008-2010 (no. 48) to the white-Kauffmann-Le minor scheme. Res Microbiol. 2014;165(7):526–30.View ArticlePubMedGoogle Scholar
  18. Ewing WH. (1986) Edwards and Ewing's identification of Enterobacteriaceae, Elsevier Science Publishing Co. Inc. New York, N.Y, 4th ed.Google Scholar
  19. Shipp CR, Rowe B. A mechanised microtechnique for salmonella serotyping. J Clin Pathol. 1980;33(6):595–7.View ArticlePubMedPubMed CentralGoogle Scholar
  20. CLSI: Performance Standards for Antimicrobial Susceptibility Testing; Twenty-Third Informational SupplementM100-S23. In., vol. 33; 2013.Google Scholar
  21. Cosby DE, Cox NA, Harrison MA, Wilson JL, Buhur RJ, Fedorka-Cray PJ. Salmonella and antimicrobial resistance in broilers:A review. J Appl Poult Res. 2015;24:408–26.View ArticleGoogle Scholar
  22. Butaye P, Michael GB, Schwarz S, Barrett TJ, Brisabois A, White DG. The clonal spread of multidrug-resistant non-typhi Salmonella serotypes. Microbes Infect. 2006;8(7):1891–7.View ArticlePubMedGoogle Scholar
  23. Antunes P, Mourao J, Campos J, Peixe L. Salmonellosis: the role of poultry meat. Clin Microbiol Infect. 2016;22(2):110–21.View ArticlePubMedGoogle Scholar
  24. Hugas M, Beloeil P. Controlling Salmonella along the food chain in the European Union - progress over the last ten years. Euro Surveill. 2014;19(19)Google Scholar
  25. Ziyate N, Karraouan B, Kadiri A, Darkaoui S, Soulay A. Prevalence and antimicrobial resistance of Salmonella isolates in Moroccan laying hens farms. J Appl Poult Res. 2016;25:539–46.View ArticleGoogle Scholar
  26. Fagbamila IO, Barco L, Mancin M, Kwaga J, Ngulukun SS, Zavagnin P, Lettini AA, Lorenzetto M, Abdu PA, Kabir J, et al. Salmonella serovars and their distribution in Nigerian commercial chicken layer farms. PLoS One. 2017;12(3):e0173097.View ArticlePubMedPubMed CentralGoogle Scholar
  27. Alali WQ, Thakur S, Berghaus RD, Martin MP, Gebreyes WA. Prevalence and distribution of Salmonella in organic and conventional broiler poultry farms. Foodborne Pathog Dis. 2010;7(11):1363–71.View ArticlePubMedGoogle Scholar
  28. Gaffga NH, Barton Behravesh C, Ettestad PJ, Smelser CB, Rhorer AR, Cronquist AB, Comstock NA, Bidol SA, Patel NJ, Gerner-Smidt P, et al. Outbreak of salmonellosis linked to live poultry from a mail-order hatchery. N Engl J Med. 2012;366(22):2065–73.View ArticlePubMedGoogle Scholar
  29. Basler C, Forshey TM, Machesky K, Erdman MC, Gomez TM, Nguyen TA, Behravesh CB. Multistate outbreak of human Salmonella infections linked to live poultry from a mail-order hatchery in Ohio--march-September 2013. MMWR Morb Mortal Wkly Rep. 2014;63(10):222.PubMedPubMed CentralGoogle Scholar
  30. Taylor M, Leslie M, Ritson M, Stone J, Cox W, Hoang L, Galanis E, Bowes V, Byrne S, de With N, et al. Investigation of the concurrent emergence of Salmonella enteritidis in humans and poultry in British Columbia, Canada, 2008-2010. Zoonoses Public Health. 2012;59(8):584–92.View ArticlePubMedGoogle Scholar
  31. Barua H, Biswas PK, Olsen KE, Christensen JP. Prevalence and characterization of motile Salmonella in commercial layer poultry farms in Bangladesh. PLoS One. 2012;7(4):e35914.View ArticlePubMedPubMed CentralGoogle Scholar
  32. Adesiyun A, Webb L, Musai L, Louison B, Joseph G, Stewart-Johnson A, Samlal S, Rodrigo S. Survey of Salmonella contamination in chicken layer farms in three Caribbean countries. J Food Prot. 2014;77(9):1471–80.View ArticlePubMedGoogle Scholar
  33. Alvarez-Fernandez E, Alonso-Calleja C, Garcia-Fernandez C, Capita R. Prevalence and antimicrobial resistance of Salmonella serotypes isolated from poultry in Spain: comparison between 1993 and 2006. Int J Food Microbiol. 2012;153(3):281–7.View ArticlePubMedGoogle Scholar
  34. Kuang X, Hao H, Dai M, Wang Y, Ahmad I, Liu Z, Zonghui Y. Serotypes and antimicrobial susceptibility of Salmonella spp. isolated from farm animals in China. Front Microbiol. 2015;6:602.PubMedPubMed CentralGoogle Scholar
  35. Zewdu E: Prevalence, distribution and antimicrobial resistance profile of Salmonella isolated from food items and personnel in Addis Ababa, Ethiopia 2004.Google Scholar
  36. Beyene T, Endalamaw D, Tolossa Y, Feyisa A. Evaluation of rational use of veterinary drugs especially antimicrobials and anthelmintics in Bishoftu, Central Ethiopia. BMC Res Notes. 2015;8:482.View ArticlePubMedPubMed CentralGoogle Scholar

Copyright

Advertisement