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Scholars
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African Journal of Pig Farming ISSN: 2375-0731 Vol. 12 (1), pp. 001-010, January, 2024. Available online at 
www.internationalscholarsjournals.org © International Scholars Journals 

 

Author(s) retain the copyright of this article. 

 
 
Full Length Research Paper 

 

Salmonella diversity and antimicrobial resistance 
in Burkina Faso: An investigation of strains from 

various sources 
 

Kagambèga A.1, 2, 3*, Bouda S. C.2, Bako E.2, Cissé H.2, Barro N.2 and Haukka K.1, 4
 

 
1
Bacteriology Unit, Department of Infectious Disease Surveillance and Control, National Institute for Health 

and Welfare (THL), Helsinki, Finland. *Corresponding author. E-mail: kagamas2007@yahoo.fr; 
kagambega.asseta@gmail.com.  

2
Laboratoire de Biologie Moléculaire, D’épidémiologie et de Surveillance des Bactéries et Virus 

Transmissibles Par Les aliments (LaBESTA)/Centre de Recherche en Sciences Biologiques, Alimentaires et 
Nutritionnelles (CRSBAN)/Ecole Doctorale Sciences et Technologies (EDST)/Université Ouaga I Professeur 

Joseph KI-ZERBO, 03 BP 7021 Ouagadougou 03, Burkina Faso.  
3
Institut Des Sciences (IDS), 01 BP 1757 Ouagadougou 01, Burkina Faso. 

4
Department of Food and 

Environmental Sciences, Division of Microbiology and Biotechnology P. O. Box 56, FI-00014 University of 
Helsinki, Finland. 

 
Accepted 25 September, 2023  

 
Epidemiologic and traceback evidence of Salmonella infection is not much in many developing 
countries including Burkina Faso. This study investigates the antimicrobial resistance and distribution 
of Salmonella serotypes isolated from diverse sources in Burkina Faso. 615 Salmonella serotypes 
isolated from beef meat, poultry carcasses, poultry, swine, cattle, hedgehog, fish, salad, channel and 
humans from 2009 to 2011 were analyzed to identify their diversity and distribution among the samples. 
The Salmonella strains were subjected to antimicrobial sensitivity tests using disk diffusion methods, 
were analyzed and classified into 110 serotypes, with the most prevalent serotype being Derby (91/615) 
found in beef meat, poultry carcasses, poultry and fish; Muenster (48/615) found in cattle, swine, 
hedgehog, poultry, human and fish; Chester (38/615) found in poultry carcasses, swine and poultry 
feces; Hato (32/615) found in beef meat, poultry carcasses, cattle and poultry; Drac (30/615) found in 
cattle, hedgehog and fish; and Typhimurium (21/615) found in cattle, poultry, human and fish. Among 
the 615 Salmonella strains, 94% (581/615) were resistant to one or more antibiotics; resistance to 
streptomycin was the most common. The resistance pattern, Str-Sul-Tet, Str-Tet and Str-Sul was 
dominant and found in 80% of the strains. About 3% of the strains were resistant to 5 or 6 antibiotics; 
their resistance pattern is amp-str-sul-tet-tmp or amp-chl-str-sul-tet-tmp. One Salmonella strain, S. 
Kentucky isolated from human stool was resistant to eight antibiotics; the resistance pattern is amp-str-
sul-tet-cip-gen-nal-mec. Findings from this study can help define the guidelines for basic surveillance 
system of Salmonella and other enteropathogenic bacteria circulating among humans, animals, food 
and environment. 

 
Key words: Salmonella, environment, human, risk.  

 
INTRODUCTION 

 
Salmonella spp. especially Non-Typhoid Salmonella 
(NTS) is a common source of foodborne diseases that 
cause morbidity and mortality worldwide (Smith et al., 

 
 
2016). It is estimated that Salmonella spp. cause 93.8 
million cases of gastroenteritis and 155,000 deaths each 
year worldwide. Approximately 86% of these cases are 



2 

 

 
 
 

 

the result of foodborne infections (Majowicz et al., 2010). 
In Burkina Faso, bacteriological results showed that the 
rate of Salmonella contamination remains quite high 
(Simporé et al., 2009). In fact, the infection progresses 
mostly periodically and rarely in an epidemic mode, and 
they are not reported due to lack of food borne pathogens 
surveillance system.  

Salmonella spp. can survive for long periods in natural 
waters, and the persistence of specific and epidemic 
strains is a great concern in public health. However, 
information on the diversity and occurrence of Salmonella 
strains is very scarce (Cui et al., 2008), making the 
ecology of these species remains unknown. Food 
animals, including poultry, pigs, and cattle are the key 
reservoirs for human salmonellosis (Hauser et al., 2011). 
In developing countries, wild and food animals are the 
sources of Salmonella distribution in water, vegetables, 
salad and the products derived from these animals due to 
lack of hygiene (Kagambèga et al., 2013). The 
emergence of antimicrobial resistant Salmonella is mostly 
associated with the non-therapeutic use of various 
classes of antimicrobials in large quantities in food 
animals (Marshall and Levy, 2011; Mir et al., 2015).  

Researchers have reported a link between the use of 
antimicrobials in food animals and the emergence of 
antimicrobial resistance in pathogenic bacteria 
(Ungemach et al., 2006; Mir et al., 2015). The increasing 
number of multidrug-resistant NTS strains is a global 
concern; this has made some countries and international 
organizations create surveillance systems which include 
collaboration between human health, veterinary, and food 
related sectors to monitor the spread of foodborne 
bacteria.  

Unfortunately, these surveillance systems are missing 
in many developing countries like Burkina Faso. The 
absence of controlled reporting of Salmonella serotypes 
through the WHO-GFN program in Burkina Faso inspired 
the compilation of data on the sporadic reporting of 
Salmonella serotypes isolated from various sources. 
Therefore, the purpose of the present study is to provide 
information on the diversity and antimicrobial resistance 
of Salmonella strains isolated from environment, animals, 
food and humans. These data will allow one to follow the 
trends in Salmonella enterica serotypes that provide 
information about sources of infection and the efficacy of 
prevention and control measures. 
 
 
MATERIALS AND METHODS 
 
Salmonella strains (n= 615) isolated from meat, poultry carcasses, 
poultry, cattle, pigs, hedgehog, water, salad and humans were 
collected in Burkina Faso from 2009 to 2011. Sampling was done 
based on the microbiological conditions. The strains were isolated  

 
 
 

 
using standard bacteriological methods and serotyped according to 
Kauffman White scheme (Kagambega et al., 2013; Bonkoungou et 
al., 2013; Traoré et al., 2015).  

Antimicrobial susceptibility of the isolates was tested by a 
standard disk diffusion method, and Escherichia coli RHE 6715 
(ATCC 25922) was used for validating the antimicrobial test results 
(CLSI, 2015). The antimicrobial agents used were ampicillin (10 
µg), chloramphenicol (30 µg), streptomycin (10 µg), sulphonamides 
(3 µg), trimethoprim (5 µg), tetracycline (30 µg), gentamicin (10 µg), 
nalidixic acid (30 µg), ciprofloxacin (5 µg), cefotaxime (30 µg), 
mecillinam (10 µg) and imipenem (10 µg). Minimal inhibitory 
concentration (MIC) for ciprofloxacin (0.002 to 32 μg/ml) was 
determined by E-test (AB Biodisk, Solna Sweden) of the isolates 
resistant to nalidixic acid. MIC breakpoint ≤ 1 μg/ml was interpreted 
as susceptible (CLSI, 2009). 
 
 
Ethics approval and consent to participate 
 
Permission to conduct this study was obtained from the 
slaughterhouse authorities and the study protocol was approved by 
the Ethical Committee of Burkina Faso. 
 

 

RESULTS AND DISCUSSION 

 

A total of 615 strains of Salmonella isolated from meat, 
poultry carcasses, poultry, cattle, pigs, hedgehog, water, 
salad and humans were distributed into 110 different 
serotypes (Table 1). The six most prevalent serotypes 
were Derby, Muenster, Chester, Drac, Hato and 
Typhimurium. Salmonella Derby (91/615) was found in 
beef meat (n=2), poultry carcasses (n= 34), poultry (n=  
52) and fish (n = 3). Our findings show that S. Derby is 
the most often isolated serotypes in poultry. This is in 
contrast with results reported by some authors, showing 
that this serotype is most common in pig and also the 4 
most frequently isolated serotype in humans in Europe 
(Kerouanton et al., 2013; Hauser et al., 2011).  

Salmonella Muenster was the second most common 
serotype and was found in cattle, swine, hedgehog, 
poultry, human and fish. This finding shows that this 
serotype is not restricted to one host but can be found in 
animals, foods, water or humans. A documented food 
poisoning outbreak caused by S. Muenster occurred in 
Canada in 1982; it infected cheddar cheese made from 
unpasteurized milk (Wood et al., 1984). Salmonella 
Chester was found in poultry carcasses, swine and 
poultry feces; this serotype has been reported in many 
countries: in Canada, S. Chester was responsible for an 
outbreak associated to frozen meals in 2010 (Taylor et 
al., 2012); in 2014, six European countries (Belgium, 
France, Spain, Germany, Sweden and the UK) reported 
S. Chester cases to the European Centre for Disease 
Prevention and Control (ECDC) associated with travel in 
Morocco (Whitworth, 2016). Salmonella Hato was found  
 

  
  



3 

 

  
 
 

 
Table 1. Salmonella serotypes and antimicrobials profile.  

 

 Salmonella Beef Poultry 
cattle swine Hedgehog Poultry Human Salad Fish Resrvoirs Channel Total 

Resistance Number of antibiotic Number of resistant 
 

 

serotypes meat carcasses pattern resistered serotype  

           
 

 S.Abaetetuba 0 0 1 0 0 1 0 0 0 0 0 2 str 1 1 
 

 S.Abony 0 0 0 0 0 1 0 0 0 0 0 1 0 0 0 
 

 S.Adabraka 0 0 0 0 0 0 0 0 0 1 0 1 str 1 1 
 

 S.Adelaide 0 1 0 0 0 1 0 0 0 0 0 2 0 0 0 
 

 S.Agona 0 4 0 0 0 3 0 0 3 0 0 10 str 1 5 
 

 S.Ahmadi 0 0 1 0 0 0 0 0 0 0 0 1 0 0 0 
 

 S.Albany 0 0 2 0 0 2 0 0 0 0 0 4 str 1 2 
 

 S.Anatum 0 1 0 0 0 1 0 0 0 0 0 2 str 1 2 
 

 S.Angers 0 0 0 0 0 0 1 0 0 0 0 1 0 0 0 
 

 S.Ank 0 0 0 0 4 1 0 0 0 0 0 5 str 1 5 
 

 S.Antwepen 0 0 1 0 0 0 0 0 0 0 0 1 str 1 1 
 

 S.Apeyeme 0 0 2 0 0 3 0 0 0 0 0 5 str 1 5 
 

 S.Banana 0 3 1 0 1 2 1 0 0 0 0 8 str 1 5 
 

 S.Bareilly 0 0 1 0 0 0 0 0 0 0 0 1 str 1 1 
 

 S.Bargny 0 0 1 0 0 0 0 0 0 0 0 1 str 1 1 
 

 S.Binningen 0 0 0 0 0 2 0 0 0 0 0 2 0 0 0 
 

 S.Bochum 0 0 0 0 0 0 0 0 2 0 0 2 0 0 0 
 

 S.Brancaster 0 1 1 0 0 3 0 0 0 0 0 5 str 1 4 
 

 S.Bredeney 1 0 5 0 0 2 0 1 6 0 1 16 str 1 4 
 

 S.Brive 0 0 1 0 0 0 0 0 1 0 0 2 str 1 1 
 

 S.Carmel 0 0 1 0 0 0 0 0 0 1 0 2 0 0 0 
 

 S.Carno 0 0 1 0 0 0 0 0 0 0 0 1 0 0 0 
 

 S.Chandans 0 0 2 0 0 0 0 0 0 0 0 2 str 1 1 
 

 S.Chester 0 5 1 0 0 31 0 0 0 0 1 38 str 1 37 
 

 S.Chomedey 0 0 4 0 0 0 0 0 0 0 0 4 str 1 4 
 

 S.Colindale 0 0 1 0 0 0 0 4 0 1 2 8 str 1 2 
 

 S.Colobane 0 0 2 0 0 0 0 0 0 0 0 2 str 1 2 
 

 S.Cubana 0 0 0 0 0 0 5 0 1 0 0 6 str 1 2 
 

 S.Dahra 0 0 2 0 0 0 0 0 0 0 0 2 str 1 1 
 

 S.Dakar 0 0 1 0 0 0 0 0 0 0 0 1 str 1 1 
 

              str,str-sul,str-   
 

 
S.Derby 2 34 0 0 0 52 0 0 3 0 0 91 

tet,str-sul- 
5 57  

 
tet,chl-str,str-  

                
 

              cip   
 

 S.Drac 0 0 26 0 1 0 0 0 3 0 0 30 str 1 20 
 

 S.Dublin 0 0 0 0 0 0 1 0 0 0 0 1 0 0 0 
 



4 

 

               
 

Table 1. Contd.                
 

                 
 

S.Duisburg  0 0 0 0 0 1 1 0 0 0 0 2 str 1 2 
 

S.Ealing  0 0 0 0 0 0 0 0 1 0 0 1 0 0 0 
 

S.Eastbourne  0 1 2 0 0 2 0 0 1 0 3 9 str 1 5 
 

S.Eastglam  0 0 0 0 0 0 0 0 2 0 0 2 0 0 0 
 

S.Elisabethville  0 0 0 0 0 0 0 0 1 0 0 1 0 0 0 
 

S.Farakan  0 0 3 0 0 0 0 0 0 0 0 3 str 1 2 
 

S.Freetown  0 0 0 0 0 1 0 0 0 0 0 1 str 1 1 
 

S.Fresno  0 0 1 0 0 4 1 0 1 0 0 7 str 1 3 
 

S.Frintrop  0 0 1 0 0 0 0 0 0 0 0 1 str 1 1 
 

S.Fufu  0 0 1 0 0 0 0 0 0 0 0 1 str 1 1 
 

S.Galiema  0 1 0 0 0 2 0 0 0 0 1 4 str 1 4 
 

S.Gaminara  0 0 0 0 0 0 1 0 0 0 0 1 0 0 0 
 

S.Gerland  0 0 0 0 0 0 0 1 0 0 0 1 str 1 1 
 

S.Give  0 0 0 0 0 0 0 0 1 0 1 2 0 0 0 
 

S.Gokul  0 0 1 0 0 0 0 0 0 0 0 1 str 1 1 
 

              str, tet,str-   
 

S.Hato 
 

1 4 5 0 0 22 0 0 0 0 0 32 
tet,sul-tet,amp- 

5 15  

 
str, amp-str-  

                
 

              sul-tet-tmp   
 

S.Havana  0 0 0 0 0 0 0 0 2 0 0 2 0 0 0 
 

S.Hermannswerder 0 0 0 0 0 0 0 0 1 0 0 1 str-sul 2 1 
 

S.Hillingdon  0 0 0 0 0 1 0 0 0 0  1 str 1 1 
 

S.Hvittingfoss  0 0 0 0 0 0 1 0 0 0 0 1 str 1 1 
 

S.Ikeja  0 0 1 0 0 0 0 0 0 0 0 1 str 1 1 
 

S.Ilala  0 0 2 1 0 0 0 0 0 0 0 3 str 1 1 
 

S.Kaapstad  0 0 0 1 0 4 0 0 0 0 0 5 str 1 2 
 

S.Kalamu  0 0 1 0 0 0 0 0 0 0 0 1 0 0 0 
 

S.Kalina  0 0 2 0 0 0 0 0 0 0 0 2 str 1 1 
 

              amp-str-sul-tet-   
 

S.Kentucky  0 0 0 0 0 0 1 0 1 0 0 2 cip-gen-nal- 8 1 
 

              mec   
 

S.Kiambu  0 0 0 0 0 0 1 0 0 0 0 1 0 0 0 
 

S.Kingston  0 0 2 0 0 3 0 0 0 0 0 5 str 1 2 
 

S.Kokomlemle  0 0 2 0 0 1 0 0 1 0 0 4 str 1 2 
 

S.Korlebu  0 0 2 0 0 0 0 4 1 0 0 7 str 1 5 
 

S.Lagos  0 0 4 0 0 2 0 0 0 0 0 6 str 1 4 
 

S.Llandoff  0 0 0 0 0 0 0 0 1 0 2 3 0 0 0 
 

S.Mbandaka  0 0 0 0 0 0 0 0 1 0 0 1 0 0 0 
 



5 

 

                
 

Table 1. Contd.                
 

                
 

S.Minnesota 0 0 0 0 0 0 0 0 1 0 0 1 0 0 0 
 

S.Moero 0 0 1 0 0 0 0 0 0 0 0 1 0 0 0 
 

S.Monschaui 2 3 1 0 3 1 0 0 0 0 0 10 str 1 7 
 

S.Montevideo 0 0 0 0 0 0 1 0 1 0 0 2 0 0 0 
 

             str, str-sul, str-   
 

S.Muenster 0 0 17 3 11 6 4 0 6 0 0 47 tet, str, str-nal, 5 20 
 

             amp-str   
 

S.Nima 0 1 3 0 0 0 0 0 0 0 0 4 0 0 0 
 

S.Nottingham 0 1 2 0 0 1 0 0 2 0 0 6 str-tet 2 1 
 

S.Offa 0 0 0 0 0 0 0 0 1 0 0 1 0 0 0 
 

S.Oranienburg 0 0 1 0 0 0 0 0 0 0 0 1 str 1 1 
 

S.Othmarschen 0 0 1 0 0 0 0 0 0 0 0 1 str 1 1 
 

S.Ouagadougou 0 0 0 0 0 0 0 0 0 0 1 1 str 1 1 
 

S.Ouakam 0 0 0 1 0 0 2 0 0 0 0 3 str 1 2 
 

S.Poona 0 0 2 0 0 1 3 0 2 1 1 10 str 1 5 
 

S.Rissen 0 0 1 0 0 0 0 0 0 0 1 2 0 0 0 
 

S.Rubislaw 0 0 0 0 0 0 1 0 0 0 0 1 0 0 0 
 

S.Ruiru 0 0 8 0 0 0 0 0 0 0 0 8 str,str-tet 2 5 
 

             str, str-tet,   
 

S.Group B 0 1 1 0 0 0 2 0 1 0 0 5 amp-chl--str- 6 4 
 

             sul-tmp   
 

S.Group C 0 1 1 0 0 9 0 0 0 0 0 11 str, str-sul 2 11 
 

S.Group¤ D 0 0 0 0 0 1 0 0 0 0 0 1 str 1 1 
 

S.Group¤ E 0 0 1 0 0 5 0 0 0 0 0 6 str, str-sul-tet 3 3 
 

S.Group¤ G 0 0 0 0 1 0 0 0 0 0 0 1 str 1 1 
 

S.Group¤ M 0 0 0 0 0 0 0 0 1 0 0 1 0 0 0 
 

S.Group¤ O:53 0 0 0 0 0 0 0 0 0 0 1 1 0 0 0 
 

S.Saarbruecken 0 1 0 0 0 0 0 0 0 0 0 1 str 1 1 
 

S.Saintpaul 0 0 0 0 0 1 0 0 0 0 0 1 0 0 0 
 

S.Salford 0 0 1 0 0 0 0 0 0 0 0 1 0 0 0 
 

S.Schwarzengrund 0 0 1 0 0 3 0 0 1 1 0 6 str 1 3 
 

S.Senftenberg 1 2 0 0 2 8 0 0 0 0 3 16 
str, str-tet, str- 

3 6  

sul-tet  

               
 

S.Shangani 0 0 0 0 0 1 0 0 0 0 0 1 str-sul 2 1 
 

S.Shubra 0 0 0 0 0 0 0 0 0 0 1 1 0 0 0 
 

S.Soerenga 0 0 0 0 0 0 1 0 0 0 0 1 0 0 0 
 

S.Soumbedioune 0 0 4 0 0 0 0 0 0 0 0 4 str 1 3 
 

S.Stanley 0 0 0 0 0 0 1 0 0 0 0 1 str 1 2 
 



6 

 

               
 

Table 1. Contd.               
 

                
 

S.Stanleyville 0 0 0 0 0 1 0 0 0 0 0 1 str-tet 2 1 
 

S.Tamberma 0 0 0 0 0 0 1 0 0 0 0 1 str-tet 2 1 
 

S.Tennessee 0 0 3 0 0 0 0 0 0 0 0 3 str 1 1 
 

S.Teshie 0 0 0 0 0 0 0 0 0 0 1 1 str 1 1 
 

S.Tilene 3 2 1 0 0 0 0 0 1 0 1 8 str 1 7 
 

S.Tounouma 0 0 0 0 0 0 1 0 0 0 0 1 str 1 1 
 

S.Trachau 0 0 1 0 0 1 0 0 0 0 0 2 str 1 2 
 

S.Typhi 0 1 0 0 0 0 1 0 0 0 0 2 
str,amp-chl-str- 

6 2  

sul-tet-tmp  

               
 

             str,amp-chl-str-   
 

S.Typhimurium 0 0 3 0 0 4 13 0 1 0 0 21 
sul-tet-tmp, 

6 21  

amp-chl-str-sul-  

               
 

             tmp   
 

S.Umbilo 0 0 1 0 0 0 0 0 0 0 0 1 str 1 1 
 

S.Urbana 0 0 13 2 0 1 0 0 0 0 0 16 
str, str-tet, chl- 

4 11  

str-tmp  

               
 

S.Vilvoorde 0 0 0 0 0 0 1 0 0 0 0 1 0 0 0 
 

S.Virchow 0 0 1 0 0 0 2 0 0 0 1 4 str 1 1 
 

S.Waedenswil 0 0 0 0 0 0 0 0 1 0 0 1 0 0 0 
 

S.Wagadugu 0 0 0 0 0 0 0 0 0 1 1 2 str 1 2 
 

S.Waycross 0 0 2 0 0 1 0 0 3 0 0 6 str 1 2 
 

S.Yoruba 0 0 1 0 0 0 0 0 0 0 0 1 str 1 1 
 

Salmonella sp. 0 0 1 0 0 0 0 0 0 0 2 3 str 1 2 
 

Total 10 68 161 8 23 193 48 10 56 6 25 608 - - 359 
 

 
amp, ampicillin; chl, chloramphenicol; str, streptomycin; sul, sulphonamides; tmp, trimethoprim; tet, tetracycline; nal, nalidixic acid; cip, ciprofloxacin; ftx, cefotaxime; mec, mecillinam. 

 
 

 

in beef meat, poultry carcasses, cattle and poultry; 
Salmonella Drac was found in cattle, hedgeghog 
and fish. Salmonella Typhimurium was found in 
cattle, poultry, human and fish. S. Typhimurium 
has been implicated in many outbreaks worldwide 
(Rayamajhi et al., 2008). This serotype has a well-
characterized ability to infect various species 
(Rabsch et al., 2002) and can survive for a long 
time in the environment (Baudart et al., 2000); 
these 2 factors enhance the ability of this serotype 
to be one of the most common causes of 

 
 
 

 

salmonellosis in many geographically diverse 
regions and has caused many disease outbreaks 
(Mather et al., 2013; Cui et al., 2008; Galanis et 
al., 2006).  

Although serotype Typhimurium was associated 
with several foods of animal origin, the most 
common was chicken (26% of outbreaks), 
indicating that chicken is a major route of 
exposure. This corroborates with our present 
results, where poultry is identified as the primary 
source of S. Typhimurium. In contrast to the report 

 
 
 

 

of Foley et al. (2008), Typhimurium was the most 
common serotype among pork associated with 
outbreaks. This shows that serotype Typhimurium 
has emerged as the predominant serotype in 
swine. After the six most prevalent serotypes, the 
presence of serotype like Typhi (poultry carcasses 
and human), Senftenberg, Virchow, Kentucky, 
Stanley and Kingston which have caused many 
outbreaks in diverse regions were noted. The 
presence of S. Typhi in poultry carcasses shows 
that there is a cross-contamination during 



7 

 

 
 
 

 

carcasses handling since humans are the only reservoir 
of typhoid Salmonella. This is also due to the fact that 
humans can be a chronic carrier of these Salmonella 
(Eng et al., 2015).  

Carriers of S. Typhi and S. Paratyphi are responsible 
for the spreading of enteric fever in endemic regions, as 
the common transmission route is the ingestion of water 
or food, contaminated with the feces of chronic carriers 
(Bhan et al., 2005). In this report, Salmonella serotypes 
Drac, Banana, Monschaui, Muenster, Seftenberg are 
found in wild hedgehogs. This animal has been the 
source of human salmonellosis in many Europeans 
countries, used as a pet animal (Nauerby et al., 2000). 
Although little can be done to prevent the spread of 
Salmonella in the environment amongst wild animals, the 
control should be done in food handling and drinking 
water.  

Our results show that the same serotype of Salmonella 
is found in diverse sources, meaning that this serotype 
can be transmitted to humans through many sources. In 
general, food animals such as swine, poultry and cattle 
are the prime sources of Salmonella infections. The major 
dissemination routes of the pathogens involve trade in 
animals and uncooked animal food products. The 
slaughtering process of food animals at abattoirs is 
considered one of the important sources of organ and 
carcass contamination with Salmonella (Gillespie et al., 
2005). In Burkina Faso, all serotypes of Salmonella can 
circulate between animals, foods, fish, water and 
humans. This happens as animals shed feces in the 
environment which rain water carries to rivers, barrages 
and channel; aquatic animals like fish can be 
contaminated by diverse microorganisms coming from 
water. In addition, wastewater and/or untreated animal 
feces are used to grow salad and other vegetable from 
gardens. Here, we can see how humans can be 
contaminated in this closed circle, since animals can 
contaminate meat, water, fish, vegetables and 
environment; the consumers are exposed to a high risk of 
contamination by Salmonella and other pathogens.  

These findings are critical because Burkina Faso is 
facing serious problems in the area of water and 
sanitation due to demographic explosion and poor urban 
planning. This problem is increasing the risk of  
environmental and human contamination. In 
Ouagadougou, the capital city of Burkina Faso, 
wastewater from channel, where we found many 
Salmonella strains, is used to irrigate vegetables from 
gardens, and animals’ feces are also used in vegetable 
crops, which is a new source of growth for poor people. 
Vegetables like salad are not nutritive media for 
microorganisms but can constitute mechanical vectors for 
transporting microorganisms to humans if hygienic 
condition in garden is not maintained well.  

Based on our findings, as seen in Figure 1, the 
Salmonella transmission routes are based on their 
diversity and sources. The diversity of possible reservoirs 

  
  

 
 

 

of infection results in significant challenges for public 
health authorities to control the infections (Dione et al., 
2011). Among the 615 strains, 94% (581/615) were 
resistant to one or more antibiotics, and resistance to 
streptomycin was the most common (Table 1). The 
resistance pattern Str-Sul-Tet, Str-Tet and Str-Sul was 
dominant and found in 80% of the strains. About 3% of 
the strains were resistant to 5 or 6 antibiotics; their 
resistance pattern was amp-str-sul-tet-tmp or amp-chl-str-
sul-tet-tmp. One Salmonella strain, S. Kentucky isolated 
from human stool was resistant to eight antibiotics with 
the pattern, amp-str-sul-tet-cip-gen-nal-mec. This 
serotype was found also in fish in this study. In contrast, 
Centre for Disease Prevention and Control (CDC) has 
reported that S. Kentucky is typically found in cattle and 
poultry (CDC, 2011).  

In this study, streptomycin resistance was found in 94% 
of the Salmonella serotypes. Majority of aminoglycosides 
are bactericidal but Salmonella use mechanisms to resist 
their antibiotic families such as expression of plasmid-
mediated aminoglycoside modifying enzymes against 
aminoglycoside (Gebreyes and Altier, 2002). The genes 
encoding theses enzymes have been found in varieties of 
Salmonella subtypes like: Agona, Typhimurium, Newport, 
Typhimurium var. Copenhagen, Kentucky, Blockely, 
Bredeney, Anatum, Derby, Give, Enteritidis, Heidelberg, 
Saint Paul, London, Saintpaul, Hadar, Heidelberg, and 
4,5,12:i: (Levings et al., 2005). In this study, resistance to 
ampicillin was observed in Salmonella serotypes: Hato, 
Kentucky, Muenster, Typhi and Typhimurium. Beta-
lactams are generally considered bactericidal; but 
Salmonella strains are now becoming resistant to 
ampicillin and methicillin due to their wide clinical use 
(Angulo et al., 2000). In Salmonella, the secretion of a 
beta-lactamase is the common mechanism of resistance 
to beta-lactamases. Several authors reported beta-
lactamases in a variety of Salmonella serotypes including 
Enteritidis, Dublin, Haadrt, Anatum, Muenchen, Stanley, 
Panama, Virchow, and Typhimurium (Gebreyes and 
Thakur, 2005; Batchelor et al., 2005).  

In the present study, Salmonella serotypes Derby, 
Hato, Muenster, Nottingham, Ruiru, Senftenberg, 
Stanleyville, Tamberna, Typhi, Urbana and Typhimurium 
were resistant to tetracycline. Resistance to tetracycline 
has been reported in several serotypes including  
Typhimurium, Saintpaul, Enteritidis, Hadar and 
Choleraesuis, Agona, Anatum, Blockley, Bredeney, 
Colorado, Derby, Give, Haardt, Heidelberg, Infantis, 
Orion, Seftenberg, (Frech and Schwarz, 2000; Pezzella 
et al., 2004). Salmonella serotypes Derby, Hato, 
Hermannswerder, Kentucky, Muenster, Senftenberg, 
Shangani, Typhi and Typhimurium were resistant to 
sulfonamide in the present study. Many authors have 
been reported resistance to sulfonamide in a wide range 
of Salmonella serotypes such as Enteritidis, Hadar, 
Heidelberg, Orion, Rissen, Agona, Albany, Derby, Djugu, 
and Typhimurium (Antunes et al., 2005; Doublet et al., 



8 

 

  
 
 
 

 
Pets and Wild animal 

 
 

 
Water (Rivers, barrage,  
channel, well, tap water) 

 
 

 

Environment (wind, 
Food 

 

Animals 
 

insects, rodents,  
 

Grass, birds) Poultry  

 
 

 
Vegetables, fish  
and other aquatic  

animals  
Foods (meat and  
meat products,  

eggs, food staff and  
other food types) 

 
 
 

 
Human 

 

 

Figure 1.Transmissions routes of Salmonella. Red color = more implicated group in 
pathogens transmission; Orange color: the second more implicated group. 

 
 

 

2004). In our report Salmonella serotypes Hato, Urbana, 
Typhi and Typhimurium were resistant to trimethoprim. 
Martinez et al. (2005) reported trimethoprim resistance in 
Salmonella serotypes Agona, Djugu, Hadar, Neport,  
Rissen Albany, Derby, and Typhimirium. 
Chloramphenicol resistance was found in Salmonella 
serotypes, Derby, Typhi, Typhimurium and Urbana.  

This finding corroborates with the report of Alcaine et 
al. (2005), where Salmonella Typhi, Agona, Derby, 
Kiambo, Albany, Newport, Haardy, Enteritidis and 
Typhimurium isolates have been found to harbor resistant 
genes for chloramphenicol. There are two mechanisms in 
which Salmonella resistance to chloramphenicol is 
conferred: (i) by the plasmid-mediated enzymes called  
chloramphenicol acetyltransferases (CAT) or 
nonenzymatic chloramphenicol resistance gene cm1A 
and (ii) Efflux pump in which the antibiotic is pumped out 
of the cell. In this study, quinolone resistance was 
observed in Salmonella serotypes Derby, Kentucky, 
Muenster and Typhimurium. The mechanisms of 
quinolone resistance for Salmonella are all 
chromosomally mediated, so the numbers of quinolone-
resistant Salmonella can only increase in two ways: (i) 
the selection of a quinolone-resistant bacterium after 
exposure to a fluoroquinolone in humans or animals, or 
(ii) the spread of a quinolone-resistant bacterium to other 

 
 
 

 

animals or to humans (Piddock, 2002). According 

to CDC, outbreaks caused by antimicrobial-resistant  
Salmonella have been associated with an increased rate 
of hospitalization, and the rate of death was significantly 
greater in outbreaks caused by resistant strains (CDC, 
2011).  

Resistance can spread from non-human sources to 
human by various routes such as animal, water and 
contaminated foods (Figure 1). Resistance to 
combinations of many classes of antimicrobial agents in 
Salmonella has led to the re-emergence of multidrug 
resistance Salmonella (MDR) strains (O’Brien, 2002). In 
this study, Salmonella serotypes, Derby, Hato, 
Hermannswerder, Urbana, Shangani, Tamberma, 
Kentucky, Muenster, Senftenberg, Shangani, Typhi and 
Typhimurium were MDR. This is similar to the findings of 
many authors, who reported that MDR Salmonella strains 
have been found to be of many serotypes such as  
Agona, Anatum, Pullorum, Schwarzengrund, 
Choleraesuis, Derby, Dublin, Heidelberg, Kentucky, 
Newport, Senftenberg, Typhimurium, and Uganda (Chen 
et al., 2004; Zhao et al., 2008). All S. Typhimurium 
reported in the present study were MDR and most of 
them were found to display a phenotype of resistance to 
ampicillin, chloramphenicol, streptomycin, sulfonamides, 
and tetracycline (ACSSuT). These antibiotics are the 



9 

 

 
 
 

 

most common drug classes used in veterinary medicine 
(Mulvey et al., 2006). 
 

 

Conclusion 

 

The genetic make-up of the Salmonella strains permits 
their adaptation in various environments, including 
human, animal and non-animal hosts. This increases the 
difficulty in eliminating the bacteria.  

Moreover, the emergence of MDR Salmonella strains 
poses a great challenge in terms of effective treatment of 
the infections caused by these strains. Several preventive 
measures have been proposed to stop the spread of 
antimicrobial resistant Salmonella infections, and the 
restriction of indiscriminate use of antibiotics in food 
animals is by far one of the most effective measures. This 
report can help international organization to understand 
Salmonella data and trends and to develop more 
informed solutions for reducing Salmonella contamination 
along the farm to table chain. The report of sporadic data 
about Salmonella serotype distribution will highlight the 
importance of the potential source of Salmonella infection 
to humans.  

The data obtained in this study can be used by the 
World Health Organization- Global Foodborne Infections 
Network (WHO-GFN) and public authority to define the 
guidelines for basic surveillance system of Salmonella 
and other enteropathogenic bacteria circulating among 
humans, animals, food and environment. 
 

 

CONFLICT OF INTERESTS 

 

The authors have not declared any conflict of interests. 
 

 

ACKNOWLEDGEMENT 

 

This research was supported by the International 
Foundation for Science (IFS) grant E/5001-2F/4600 to 
AK. The efforts of all who contributed to the success of 
the research are highly appreciated, ranging from 
conducting of strain characterization and drafting of the 
manuscript, as well as supervision and participation in 
writing of the manuscript. All authors read, commented on 
and approved of the final manuscript. 
 
 
REFERENCES 
 
Alcaine SD, Sukhnanand SS, Warnick LD, Su WL, McGann P, 

McDonough P, Wiedmann M (2005). Ceftiofur-resistant Salmonella 
strains isolated from dairy farms represent multiple widely distributed 
subtypes that evolved by independent horizontal gene transfer. 
Antimicrob. Agents Chemother. 49:4061-4067.  

Angulo FJ, Johnson KR, Tauxe RV, Cohen ML (2000). Origins and 
consequences of antimicrobial-resistant nontyphoidal Salmonella: 
implications for the use of fluoroquinolones in food animals. Microb. 
Drug Resist. 6:77-83. 

  
  

 
 

 
Antunes P, Machado J, Sousa JC, Peixe L (2005). Dissemination of 

sulfonamide resistance genes (sul1, sul2, and sul3) in Portuguese 
Salmonella enterica strains and relation with integrons. Antimicrob. 
Agents Chemother. 49:836-839. 

Batchelor M, Hopkins K, Threlfall EJ, Clifton-Hadley FA, Stallwood AD, 
Davies RH, Liebana E (2005). bla(CTX-M) genes in clinical 
Salmonella isolates recovered from humans in England and Wales 
from 1992 to 2003. Antimicrob. Agents Chemother. 49:1319-1322.  

Baudart J, Lemarchand K, Brisabois A, Lebaron P (2000). Diversity of 
Salmonella strains isolated from the aquatic environment as 
determined by serotyping and amplification of the ribosomal DNA 
spacer regions. Appl. Environ. Microbiol. 66:1544-1552. 

Bhan MK, Bahl R, Bhatnagar S (2005). Typhoid and paratyphoid fever.  
Lancet 366:749-762.  

Bonkoungou IJO, Haukka K, Österblad M, Hakanen AJ, Traoré AS, 
Barro N, Siitonen A (2013). Bacterial and viral etiology of childhood 
diarrhea in Ouagadougou, Burkina Faso. BMC Pediatr. 13:1-6.  

Centers for Disease Control and Prevention (CDC) (2011). Vital signs: 
incidence and trends of infection with pathogens transmitted 
commonly through food-Foodborne Diseases Active Surveillance 
Network, 10 U.S. sites, 1996–2010. MMWR Morb. Mortal Wkly. Rep. 
60:749-755.  

Chen S, Zhao S, White DG, Schroeder CM, Lu R, Yang H, McDermott 
Patrick F, Ayers S, Meng J (2004). Characterization of multiple-
antimicrobial-resistant Salmonella serovars isolated from retail meats. 
Appl. Environ. Microbiol. 70:1-7.  

Cui S, Li J, Sun Z, Hu C, Jin S, Guo Y, Ran L, Ma Y (2008). 
Ciprofloxacin-resistant Salmonella enterica serotype Typhimurium, 
China. Emerg. Infect. Dis. 14:493-495.  

Dione MM, Ikumapayi UN, Saha D, Mohammed NI, Geerts S, Ieven M, 
Adegbola RA, Antonio M (2011). Clonal differences between non-
typhoidal Salmonella (NTS) recovered from children and animals 
living in close contact in the Gambia. PLoS Negl. Trop. Dis. 5:1148.  

Doublet B, Butaye P, Imberechts H, Boyd D, Mulvey M R, Chaslus - 
Dancla E. Cloeckaert A (2004). Salmonella genomic island 1 
multidrug resistance gene clusters in Salmonella enterica serovar 
Agona isolated in Belgium in 1992 to 2002. Antimicrob. Agents 
Chemother. 48:2510-2517.  

Eng SK, Pusparajah P, Ab Mutalib NS, Ser HL, Chan KG, Lee LH 
(2015). Salmonella: A review on pathogenesis, epidemiology and 
antibiotic resistance. Front. Life Sci. 8:284-293.  

Foley SL, Lynne AM, Nayak R (2008). Salmonella challenges: 
prevalence in swine and poultry and potential pathogenicity of such 
isolates. J. Anim. Sci. 86:E149-62.  

Frech G, Schwarz S (2000). Molecular analysis of tetracycline 
resistance in Salmonella enterica subsp. enterica serovars 
Typhimurium, Enteritidis, Dublin, Cholerasuis, Hadar and Saintpaul: 
construction and application of specific gene probes. J. Appl. 
Microbiol. 89:633-641.  

Galanis E, Wong DMALF, Patrick ME, Binsztein N, Cieslik A, 
Chalermchaikit T, Aidara-Kane A, Ellis A, Angulo FJ, Wegener HC 
(2006). Web-based surveillance and global Salmonella distribution, 
2000-2002. Emerg. Infect. Dis. 12:381-388.  

Gebreyes WA, Thakur S (2005). Multidrug-resistant Salmonella enterica 
serovars Muenchen from pigs and humans and potential interserovar 
transfer of antimicrobial resistance. Antimicrob. Agents Chemother. 
49:503-511.  

Gebreyes WA, Altier C (2002). Molecular characterization of multidrug-
resistant Salmonella enterica subsp. enterica serovar Typhimurium 
isolates from swine. J. Clin. Microbiol. 40:2813-2822.  

Gillespie IA, O’Brien SJ, Adak GK, Ward LR, Smith HR (2005). 
Foodborne general outbreaks of Salmonella Enteritidis phage type 4 
infections, England and Wales, 1992–2002: where are the risks? 
Epidemiol. Infect. 133:759-801.  

Hauser E, Hebner F, Tietze E, Helmuth R, Junker E, Prager R, 
Schroeter A, Rabsch W, Fruth A, Malorny B (2011). Diversity of 
Salmonella enterica serovar Derby isolated from pig, pork and 
humans in Germany. Int. J. Food Microbiol. 151:141-149.  

Kagambega A, Lienemann T, Aulu L, Traoré AS, Barro N, Siitonen A, 
Haukka K (2013). Prevalence and characterization of Salmonella 
enterica from the feces of cattle, poultry, swine and hedgehogs in 
Burkina Faso and their comparison to human Salmonella isolates. 



10 

 

 
 
 

 
BMC Microbiol. 13:253.  

Kerouanton A, Rose V, Weill F-X, Granier SA, Denis M (2013). Genetic 
diversity and antimicrobial resistance profiles of Salmonella enterica 
serotype derby isolated from pigs, pork, and humans in France. 
Foodborne Pathog. Dis. 11:977-984.  

Levings RS, Lightfoot D, Partridge SR, Hall RM, Djordjevic SP (2005). 
The genomic island SGI1, containing the multiple antibiotic resistance 
region of Salmonella enterica serovar Typhimurium DT104 or variants 
of it, is widely distributed in other S. enterica serovars. J. Bacteriol. 
187:4401-4409.  

Majowicz SE, Musto J, Scallan E, Angulo FJ, Kirk M, O'Brien SJ, Jones 
TF, Fazil A, Hoekstra RM (2010). The global burden of non-typhoidal 
Salmonella gastroenteritis. Clin. Infect. Dis. 50:882-889.  

Marshall BM, Levy SB (2011). Food animals and antimicrobials: impacts 
on human health. Clin. Microbiol. Rev. 24:718-733.  

Martinez N, MendozaM C, Guerra B, Gonzalez-Hevia MA. Rodicio MR 
(2005). Genetic basis of antimicrobial drug resistance in clinical 
isolates of Salmonella enterica serotype Hadar from a Spanish 
region. Microb. Drug Resist. 11:185-193.  

Mather AE, Reid SW, Maskell DJ, Parkhill J, Fookes MC, Harris SR, 
Brown DJ, Coia JE, Mulvey MR, Gilmour MW, Petrovska L, de Pinna 
E, Kuroda M, Akiba M, Izumiya H, Connor TR, Suchard MA, Lemey 
P, Mellor DJ, Haydon DT, Thomson NR (2013). distinguishable 
epidemics of multidrug-resistant Salmonella Typhimurium DT104 in 
Different Hosts. Science 341:1514-1517.  

Mir IA, Kashyap SK, Maherchandani S (2015). Isolation, serotype 
diversity and antibiogram of Salmonella enterica isolated from 
different species of poultry in India. Asian Pac. J. Trop. Biomed. 
5:561-567.  

Mulvey MR, Boyd DA, Olson AB, Doublet B, Cloeckaert A (2006). The 
genetics of Salmonella genomic island 1. Microbes Infect. 8:1915-
1922.  

Nauerby B, Pedersen K, Dietz HH, Madsen M (2000). Comparison of 
Danish Isolates of Salmonella enterica Serovar Enteritidis PT9a and 
PT11 from Hedgehogs (Erinaceus europaeus) and Humans by 
Plasmid Profiling and Pulsed-Field Gel Electrophoresis Comparison 
of Danish Isolates of Salmonella enterica Serovar. J. Clin. Microbiol. 
38:3631-3635.  

O'Brien TF (2002). Emergence, spread, and environmental effect of 
antimicrobial resistance: How use of an antimicrobial anywhere can 
increase resistance to any antimicrobial anywhere else. Clin. Infect 
Dis. 34:78-84.  

Pezzella C, Ricci A, DiGiannatale E, Luzzi I, Carattoli A (2004). 
Tetracycline and streptomycin resistance genes, transposons, and 
plasmids in Salmonella enterica isolates from animals in Italy. 
Antimicrob. Agents Chemother. 48:903-908.  

Piddock LJV (2002). Fluoroquinolone resistance in Salmonella serovars 
isolated from humans and food animals. FEMS Microbiol. 26:3-16. 

 
 
 
 

 
Rabsch W, Andrews HL, Kingsley RA, Prager R, Tschäpe H, Adams 

LG, Bäumler AJ (2002). Salmonella enterica serotype Typhimurium 
and its host adapted variants. Infect Immun. 70:2249-55.  

Rayamajhi N, Kang S, Kang ML, Lee HS, Park KY, Yoo HS (2008). 
Assessment of antibiotic resistance phenotype and integrons in 
Salmonella enterica serovar Typhimurium isolated from swine. J. Vet. 
Med. Sci. 70:1133-1137.  

Clinical and Laboratory Standards Institute (2015) Methods for Dilution 
Antimicrobial Susceptibility Tests for Bacteria that Grow Aerobically.  

Smith S, Braun S, Akintimehin F, Fesobi T, Bamidele M, Coker A, 
Monecke S, Ehricht R (2016). Serogenotyping and antimicrobial 
susceptibility testing of Salmonella spp. isolated from retail meat 
samples in Lagos, Nigeria. Mol. Cell. Probes 30:189-194.  

Taylor J, Galanis E, Wilcott L, Hoang L, Stone J, Ekkert J, Quibell D, 
Huddleston M, McCormick R, Whitfield Y, Adhikari B, Grant CC, 
Sharma D (2012). An outbreak of Salmonella Chester infection in 
Canada: rare serotype, uncommon exposure, and unusual population 
demographic facilitate rapid identification of food vehicle. J. Food 
Prot. 75:738-742.  

Traoré O, Nyholm O, Siitonen A, Bonkoungou IJO, Traoré AS, Barro N, 
Haukka K (2015). Prevalence and diversity of Salmonella enterica in 
water, fish and lettuce in Ouagadougou, Burkina Faso. BMC 
Microbiol. 15:151.  

Ungemach FR, Müller-Bahrdt D, Abraham G (2006). Guidelines for 
prudent use of antimicrobials and their implications on antibiotic 
usage in veterinary medicine. Int. J. Med. Microbiol. 296:33-38.  

Whitworth J (2016). Studies highlight past and present Salmonella 
outbreaks. Breaking news on food safety and quality control.  
Available at 
www.foodqualitynews.com/Article/2016/06/16/Salmonella-outbreak-
studies-presented-at-symposium.  

Wood DS, Collins-Thompson DL, Irvine DM, Myhr AN (1984). Source 
and persistence of Salmonella Muenster in naturally contaminated 
Cheddar cheese. J. Food Prot. 47:20-22.  

Zhao S, White DG, Friedman SL, Glenn A, Blickenstaff K, Ayers SL, 
Abbott JW, Hall-Robinson E, McDermott PF (2008). Antimicrobial 
resistance in Salmonella enterica serovar Heidelberg isolates from 
retail meats, including poultry, from 2002 to 2006. Appl. Environ. 
Microbiol. 74:6656-6662. 


