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Genome analysis of Salmonella strains isolated from imported frozen fish in Burkina Faso

Genome analysis of Salmonella strains isolated from imported frozen fish in Burkina Faso Purpose: Fish is an excellent source of protein and vitamins for humans, but improperly handled, fish can expose consumers to pathogenic bacteria. This study was aimed to isolate and characterize the genomes of Salmonella strains isolated from imported fish sold in the open market in Ouagadougou. Methods: One hundred and fifty-nine fish were collected from open markets and were cultured for Salmonella. Antimicrobial susceptibility was determined by broth microdilution. Whole-genome sequencing was done to further study antibiotic resistance genes, plasmid replicons, and MSLT types. Serotyping was done using SeqSero 2. Result: Out of the 159 fish samples analyzed, 30 (18.9%) were found to be contaminated with Salmonella. Among the isolated Salmonella strains, six different serotypes, Nima, Liverpool, Kokomlemle, Teshie, Derby, and Tennessee, were found using SeqSero2. Salmonella Tennessee was the predominant serotype. All the isolates possessed at least one resistance gene. The aac6-Iaa aminoglycoside resistance gene was the most prevalent gene found in the strains. The gene fosA7 was detected in three strains. All the S. Nima isolates were of Multilocus Sequence Type (MLST) 8086, S. Teshie isolate was ST 530; Liverpool was ST 1959; Derby was ST 7880; Kokomlemle was ST 2696. The Tennessee isolates gave two different STs including ST 8395 and 8398. Conclusion: The presented results highlight the prevalence of Salmonella on imported fish purchased from the open markets. More attention should be paid regarding fish selling conditions in the country to prevent the potential health risk for consumers. Keywords: Salmonella, Antimicrobial resistance, Serotype, Fish Introduction has increased exponentially in this country with more Burkina Faso is a landlocked tropical country located than 96% of commercially sold fish imported from in sub-Saharan Africa. This country is characterized another country (Ministry of economic and sustain- by a dry season from October-May with hot able development, Burkina Faso. Statistique doua- temperature (35-45 °C) and a short rainy season nieres 2015). Fish is an important source of essential (June-September). In recent years, fish consumption amino acids and good fatty acids for humans, but fish can be contaminated by pathogenic bacteria that pose * Correspondence: kagambega.asseta@gmail.com; kagamas2007@yahoo.fr a high risk for consumer’s health (Yan et al. 2010; Bacterial Epidemiology and Antimicrobial Resistance Research Unit, U.S. Nwiyi and Onyeabor 2012). These pathogenic bacteria National Poultry Research Center, USDA, ARS, Athens, Georgia, USA Laboratoire de Biologie Moléculaire, d’épidémiologie et de surveillance des can contaminate ready to eat fish product through bactéries et virus transmissibles par les aliments (LaBESTA)/Ecole Doctorale cross-contamination during fish processing (Kris- Sciences et Technologies (EDST), Université Joseph KI-ZERBO, Ouagadougou, Etherton et al. 2002). Burkina Faso Full list of author information is available at the end of the article © The Author(s). 2021 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. Kagambèga et al. Annals of Microbiology (2021) 71:32 Page 2 of 8 Salmonella is a gram-negative foodborne pathogen were placed into a stomacher bag containing 90 mL of and has been implicated in fish outbreaks worldwide buffered peptone water (Liofilchem, Teramo, Italy) and (Barrett et al. 2017; Amagliani et al. 2012). More than homogenized (400 Circulator, Seward, London, UK) for 2500 serotypes of Salmonella have been designated 1 min, then incubated for 24 h at 37 °C. From this non- based on the O and H surface antigens (Issenhuth-Jean- selective pre-enrichment, 0.1 mL were transferred into jean et al. 2014). Several serotypes, including Enteritidis 10 mL of Rappaport-Vassiliadis broth (Oxoid, Basing- and Typhimurium, have been implicated in outbreaks stoke, England) and incubated for 24 h at 42 °C. A loop- associated with seafood sources, though data from Africa ful from the selective enrichment broth was streaked is limited (Amagliani et al. 2012). onto XLD (Oxoid, Basingstoke, England) agar and incu- Currently, the use of antibiotics in aquaculture prac- bated for 24 h at 37 °C. Suspected colonies on selective tices as growth promoters or for treatment and preven- agar plates were purified and bio-typed by using bio- tion of fish diseases is increasing the risk of development chemical tests and API 20E strips (BioMerieux, Marcy of antibiotic resistant bacteria among the microbiome of l’Etoile, France). fish gut and/or fishing water (Miranda et al. 2018). Many Confirmed colonies were sent to the United States De- studies have shown widespread transmission of partment of Agriculture, Agricultural Research Service, antibiotic-resistant bacteria of the fish or aquatic envir- Bacterial Epidemiology and Antimicrobial Resistance Re- onment to humans (Gonzalez-Escalona et al. 2005; search Unit for future analysis. Sørum 2006). According to the Centers for Disease Control and Pre- Antimicrobial susceptibility testing vention (CDC), antibiotic-resistant infection is respon- The isolates were streaked onto Tryptic Soy Agar (TSA) sible for 25,000 annual deaths in the European Union with 5% Sheep blood (BA), (Fisher Scientific, USA) and 23,000 annual deaths in the USA (Center for Dis- plates and incubated for 24 h at 37 °C, and one colony ease Control and Prevention (CDC) 2019). The World from each plate was streaked onto a second BA2 plate Health Organization (WHO) reported that the burden of for another 24 h at 37 °C. Minimum inhibitory concen- food-borne disease is similar to the burden of malaria, trations (MIC, μg/mL) of all Salmonella isolates were tuberculosis, and even HIV/AIDS and is disproportion- determined by broth-microdilution using the Sensititre™ ately borne by the least developed countries and by chil- semi-automated antimicrobial susceptibility system dren (World Health Organization (WHO) 2015). Since (TREK Diagnostic Systems Inc., Cleveland, OH, USA) imported fish is widely consumed in Burkina Faso, it is and the Sensititre™ Gram-Negative plate format, GN4F, important to know the microbiological quality of these (ThermoFisher Scientific, USA), according to manufac- fish. Therefore, the present study aims to understand the turer’s directions. MICs of the isolates for 24 antimicro- epidemiology and antibiotic resistance of Salmonella bials were determined using colonies from the BA2 strains isolated from fish using whole-genome sequen- plates, and each isolate was classified as resistant, inter- cing and phenotypic methods. mediate, or susceptible to the antimicrobials tested using the breakpoints set by Clinical and Laboratory Standards Materials and methods Institute (CLSI) (2016). Antimicrobials used breakpoints −1 Sampling were as follows: Amikacin (≥ 64 μgmL ); Piperacillin/ −1 Imported fish samples were purchased from different tazobactam (≥ 128/4 μgmL ); Tigecycline (≥ 1 μg −1 −1 open markets. All fish samples during collection were mL ); Ticarcillin/clavulanic acid (≥ 128/2 μgmL ); −1 first placed in sterile polypropylene bags, then placed in Levofloxacin (≥ 2 μgmL ); Nitrofurantoin (≥ 128 μg −1 −1 polystyrene boxes containing crushed ice and stored at 4 mL ); Tetracycline (≥ 16 μgmL ); Doripenem (≥ 4 μg −1 −1 °C during transportation. The samples were transported mL ); Minocycline (≥ 16 μgmL ); Ertapenem (≥ 2 μg −1 to the laboratory and processed on the same day for the mL ); Trimethoprim/sulfamethoxazole (≥ 4/76 μg −1 −1 presence of Salmonella spp. mL ); Imipenem (≥ 4 μgmL ); Piperacillin (≥ 128 μg −1 −1 mL ); Meropenem (≥ 4 μgmL ); Gentamicin (≥ 16 μg −1 −1 Bacteriological analysis mL ); Cefazolin (≥ 8 μgmL ); Tobramycin (≥ 16 μg −1 −1 Salmonella strains were isolated from fish samples fol- mL ); Ceftazidime (≥ 16 μgmL ); Ampicillin/sulbac- −1 −1 lowing the methodologies described in the International tam (≥ 32/16 μgmL ); Aztreonam (≥ 16 μgmL ); −1 −1 Organization for Standardization 6579-2017 (Inter- Ampicillin (≥ 32 μgmL ); Cefepime (≥ 32 μgmL ); −1 −1 national Organization for Standardization (ISO) 6579-1 Ciprofloxacin (≥ 4 μgmL ); Ceftriaxone (≥ 4 μgmL ). 2017). The fish samples were gently removed from For the analysis, isolates identified as intermediate were coolers and processed using aseptic conditions. The gills, considered susceptible to the drug. Escherichia coli intestines, and skin were removed using sterile knives. ATCC 25922, Pseudomonas aeruginosa ATCC 27853, About 10 g of samples (fish gills, intestines, and skin) Enterococcus faecalis ATCC 29212, and Staphylococcus Kagambèga et al. Annals of Microbiology (2021) 71:32 Page 3 of 8 aureus ATCC 29213 were controls for determination of and the assembly statistics are shown in Table 1. Among MIC. the isolated Salmonella strains, six different named sero- For each isolate, a final inoculum of 5 × 10 CFU/ml types, including Nima, Liverpool, Kokomlemle, Teshie, was targeted. The panels were read after 18 h of incuba- Derby, and Tennessee were found, with five having no tion at 35 °C. name and only antigenic formulas. Salmonella Tennes- see was the predominant serotype. All the isolates pos- Whole-genome sequencing sessed at least one resistance gene. The non-functional Genomic DNA was isolated using the GenElute bacterial aac6-Iaa conferring resistance to aminoglycosides was genomic DNA kit (Sigma-Aldrich, St. Louis, MO, USA) the most prevalent gene found in the strains. The gene following instructions for Gram-negative bacteria. Cul- fosA7 conferring resistance to Fosfomycin was detected tures were grown in 5 mL of Luria-Bertani Broth, Miller in three strains. The isolates were susceptible to all (Difco™, Becton Dickinson and Company, Sparks, MD) drugs tested using phenotypic method. Four S. Nima overnight at 37 °C with shaking. The extracted DNA isolates were identified from the 30 isolates and were all quality was read using NanoDrop 2000c spectrophotom- MLST Sequence Type (ST) 8086. One S. Teshie isolate eter (Thermo, Fisher Scientific, USA). DNA was stored was identified and was ST 530; three S. Liverpool isolates at −20 °C prior to library preparation. were detected and were identified as ST 1959; one S. Extracted DNA was quantified using the Qubit Derby isolate was found and was ST 7880; one S. double-stranded DNA (dsDNA) high-sensitivity (HS) Kokomlemle was detected and was ST 2696, 15 S. Ten- assay kit according to the manufacturer’s instructions nessee isolates were found, 14 have one of two different (Life Technologies, Inc., USA). The Illumina libraries sequence types, ST 8395 and 8398, and one was un- were prepared using the Nextera XT DNA library prep- known. Plasmid replicon typing results showed six iso- aration kit and Nextera XT index primers (Illumina, lates possessing plasmids: IncFIB and IncFII in the USA). The library fragment size distribution was Teshie isolate, Col(pHAD28) and Col4401 in three Liv- checked using the Bioanalyzer 2100 with an Agilent HS erpool isolates, Col (MG828) in one Tennessee isolate, DNA kit (Agilent Technologies, USA) and quantified and IncFII(S) in one Kokomlemle (Table 2). using a Qubit DNA HS assay kit in a Qubit fluorometer The whole-genome shotgun project has been depos- (Thermo, Fisher Scientific, USA). The generated libraries ited at GenBank under BioProject number were then sequenced using a MiSeq version 2 reagent PRJNA713376 (https://www.ncbi.nlm.nih.gov/bioproject/ kit with 500 or 300 cycles, depending on fragment size. PRJNA713376), and the accession numbers are listed in The paired-end read length of 2 × 250 bp was used for Table 2. The versions described in this paper are the 500 cycles and 2 × 150 bp for 300 cycles on the Illumina first versions. MiSeq platform. The quality metrics of the reads were performed by FastQC (http://www.bioinformatics. Discussion babraham.ac.uk/projects/fastqc/). The sequence data The present study was initiated to determine the micro- were assembled using the A5-miseq assembler (Coil biological quality of imported and local fish consumed et al. 2015), and the genome sequence was annotated via in the city of Ouagadougou, Burkina Faso. The preva- the NCBI Prokaryotic Genome Annotation Pipeline lence of Salmonella strains was 18.9% from imported (Tatusova et al. 2016). fish. This result could be explained by the fact that imported fish are exposed to several stages of handling Identification of antibiotic resistance genes, chromosomal and packaging at the farm in the country of origin, mutations, serotypes, MLST, and plasmid from total transport to Burkina Faso, reception at wholesalers, de- genome sequence livery to semi-wholesalers, and delivery to different re- SeqSero 2 was used to determine the serotypes of Sal- tailers. All these steps undoubtedly favor the monella strains from genome assembly data. Using the contamination by bacteria like Salmonella. However, the Center for Genomic Epidemiology web tools, antibiotic consumption of imported fish is very high in Burkina resistance genes were identified using ResFinder 4.1 Faso because it is very accessible and inexpensive in all (Zankari et al. 2012). MLST sequence type was identified the localities of the country. In these localities, the using MLST 2.0 (Larsen et al. 2012), and plasmids were imported fish is cut into small pieces by small traders detected using PlasmidFinder 2.0 (Carattoli et al. 2014). and sold at a minimum price of 50 FCFA (about one cent of dollar). This necessitates permanent monitoring Results of the prevalence of germs that can affect the health of Out of the 159 fish samples analyzed, 30 (18.9%) were consumers as well as chemicals. The population of Bur- found to be contaminated with Salmonella. From these kina Faso is over 80% illiterate, which will undoubtedly 30 isolates, whole-genome sequences were generated lead to an increase in contamination of raw fish and the Kagambèga et al. Annals of Microbiology (2021) 71:32 Page 4 of 8 Table 1 Assembly statistics of Salmonella strains Isolate Contigs Scaffolds Genome Longest N50 Raw EC % reads Raw nt EC nt % nt Raw EC Median 10th Bases ≥ % ID size scaffold reads reads passing EC passing EC cov cov cov percentile cov Q40 GC 87 61 61 4621725 703602 292745 2075760 2055651 99.03 3.9E+08 3.6E+08 93.77 83.55 78.35 82 59 4617943 52.2 88 61 61 4654102 433362 231906 2480308 2461694 99.25 3.5E+08 3.4E+08 97.2 74.39 72.31 73 54 4651947 52.2 89 180 180 5345366 265739 89976 1585778 1571781 99.12 2.1E+08 2E+08 96.96 39.18 37.99 37 24 5332372 51.8 95 40 40 4680005 668083 504361 2410566 2379641 98.72 4.7E+08 4.4E+08 92.32 100.7 93.01 97 72 4679387 52.2 98 63 63 4918496 775042 398010 1718264 1687773 98.23 3.3E+08 3.1E+08 92.42 67.53 62.41 65 46 4916559 51.9 100 80 80 4963160 748091 287769 2265232 2202986 97.25 4.4E+08 3.9E+08 88.29 89.07 78.65 85 62 4961107 52 101 52 52 4902134 944301 501799 1868462 1821376 97.48 3.8E+08 3.4E+08 90.4 77.46 70.02 74 54 4900597 51.8 103 49 49 4749239 1151741 340547 2323594 2296420 98.83 4.5E+08 4.2E+08 93.23 93.97 87.61 87 63 4748210 52.2 108 44 44 4738594 568197 405801 2091224 2069633 98.97 3.6E+08 3.5E+08 95.15 76.54 72.83 74 55 4737525 52.2 111 47 47 4741632 568232 454680 2514870 2487391 98.91 4.9E+08 4.5E+08 92.81 102.4 95.07 99 76 4740854 52.2 113 49 49 4749008 1444467 340548 2281594 2260595 99.08 4.6E+08 4.3E+08 93.21 97.31 90.7 92 69 4748045 52.2 116 38 38 4661074 871623 424548 1877226 1855294 98.83 3.6E+08 3.3E+08 92.87 76.86 71.37 74 54 4659622 52.2 117 44 44 4739093 568232 427385 2101626 2085634 99.24 3.6E+08 3.5E+08 95.73 76.7 73.42 74 55 4738049 52.2 119 51 51 4730026 508935 323835 1916062 1891245 98.7 2.5E+08 2.4E+08 97.36 52 50.62 50 35 4728141 52.2 122 64 64 4732251 461578 226770 2578950 2550077 98.88 3.4E+08 3.3E+08 96.81 72.58 70.26 71 49 4730117 52.2 127 46 46 4740433 568232 394001 1464044 1447638 98.88 2.6E+08 2.4E+08 95.1 53.95 51.31 52 36 4738090 52.2 128 52 52 4729542 454349 323835 1476660 1454883 98.53 1.9E+08 1.8E+08 97.27 39.56 38.48 38 26 4726471 52.2 129 43 43 4617569 720868 300407 1313142 1295563 98.66 2.4E+08 2.2E+08 93.89 51.58 48.43 50 34 4614768 52.2 130 43 43 4740056 568232 400228 3575342 3520930 98.48 6.6E+08 6E+08 91.2 138.7 126.5 133 101 4739679 52.2 131 53 53 4741832 568232 394156 1566306 1545820 98.69 2.9E+08 2.7E+08 91.49 62.2 56.91 60 42 4739118 52.2 134 34 34 4797111 1850190 750647 2710124 2671347 98.57 5.3E+08 4.8E+08 91.32 110.4 100.8 106 78 4796675 52.2 135 54 54 4903282 944125 424401 2061468 1996430 96.85 3.7E+08 3.3E+08 87.78 75.59 66.35 71 50 4901400 51.8 136 46 46 4747148 857353 340487 1895802 1849828 97.57 3.3E+08 3E+08 90 69.25 62.33 63 43 4745627 52.2 137 44 44 4739464 514012 394016 2219520 2160947 97.36 4.1E+08 3.6E+08 88.01 87.08 76.64 83 60 4738438 52.2 138 42 42 4617148 720868 331382 1581084 1563497 98.89 3.1E+08 2.8E+08 90.95 67.5 61.39 65 46 4615739 52.2 139 45 45 4740410 514012 394637 2120290 2100494 99.07 3.8E+08 3.6E+08 94.39 80.57 76.06 78 56 4739354 52.2 141 71 71 4730418 434837 164778 1976130 1952830 98.82 2.7E+08 2.6E+08 96.44 56.5 54.49 55 39 4726407 52.2 142 45 45 4620013 720868 387756 2282854 2264502 99.2 4.4E+08 4.1E+08 93.92 95.63 89.81 93 68 4619149 52.2 144 688 688 5699254 126378 26527 1655604 1640692 99.1 3.3E+08 3.1E+08 93.14 58.29 54.29 58 27 5652021 51.6 146 385 385 5031347 222688 74906 2781576 2757394 99.13 3.7E+08 3.6E+08 97.48 72.79 70.96 73 46 4988376 52.1 Kagambèga et al. Annals of Microbiology (2021) 71:32 Page 5 of 8 Table 2 Distribution of plasmid replicons and MLSTs of Salmonella from fish Sample ID Serotype Antimicrobial resistances genes Plasmid replicon MLST (ST) ParC mutation Accession numbers 87 Nima aac(6′)-Iaa 0 8086 Thr57Ser SAMN18249072 88 Tennessee aac(6′)-Iaa; fosA7 0 8395 Thr57Ser SAMN18249073 89 Teshie aac(6′)-Iaa IncFIB, IncFII 530 - SAMN18249074 95 Derby aac(6′)-Iaa 0 7880 Thr57Ser SAMN18249075 98 I 39:z10:e,n,z15 aac(6′)-Iaa 0 8401 Thr57Ser SAMN18249076 100 I 30:y:- aac(6′)-Iaa 0 8397 Thr57Ser SAMN18249077 101 I 13:i:z6 aac(6′)-Iaa 0 8396 - SAMN18249078 103 Liverpool aac(6′)-Iaa Col(pHAD28), Col4401 1959 Thr57Ser SAMN18249079 108 Tennessee aac(6′)-Iaa 0 8398 Thr57Ser SAMN18249080 111 Tennessee aac(6′)-Iaa 0 8398 Thr57Ser SAMN16842897 113 Liverpool aac(6′)-Iaa Col(pHAD28), Col4401 1959 Thr57Ser SAMN18249081 116 Tennessee aac(6′)-Iaa; fosA7 0 8395 Thr57Ser SAMN18249082 117 Tennessee aac(6′)-Iaa 0 8398 Thr57Ser SAMN18249083 119 Tennessee aac(6′)-Iaa 0 8398 Thr57Ser SAMN18249084 122 Tennessee aac(6′)-Iaa 0 8398 Thr57Ser SAMN18249085 127 Tennessee aac(6′)-Iaa 0 8398 Thr57Ser SAMN18249086 128 Tennessee aac(6′)-Iaa 0 8398 Thr57Ser SAMN18249087 129 Nima aac(6′)-Iaa 0 8086 Thr57Ser SAMN18249088 130 Tennessee aac(6′)-Iaa 0 8398 Thr57Ser SAMN18249089 131 Tennessee aac(6′)-Iaa Col(MG828) 8398 Thr57Ser SAMN18249090 134 Kokomlemle aac(6′)-Iaa IncFII(S) 2696 Thr57Ser SAMN18249091 135 I 13:i:z6 aac(6′)-Iaa 0 8396 - SAMN18249092 136 Liverpool aac(6′)-Iaa Col(pHAD28), Col4401 1959 Thr57Ser SAMN18249093 137 Tennessee aac(6′)-Iaa 0 8398 Thr57Ser SAMN18249094 138 Nima aac(6′)-Iaa 0 8086 Thr57Ser SAMN18249095 139 Tennessee aac(6′)-Iaa 0 8398 Thr57Ser SAMN18249096 141 Tennessee aac(6′)-Iaa 0 8398 Thr57Ser SAMN18249097 142 Nima aac(6′)-Iaa 0 8086 Thr57Ser SAMN18249098 144 I 39:f,g:e,n,z15 aac(6′)-Iaa 0 Unknown Thr57Ser SAMN18249099 146 Tennessee aac(6′)-laa, fosA7 0 Unknown Thr57Ser SAMN16842913 Less than 100% identity Nearest STs: 384, 696, 1859, 2320, 4924, 5805, 6540, 6730, 6732, 6734 Nearest ST: 8398 possibility of cross-contamination due to a lack of train- missing (Barro et al. 2008; Kagambèga et al. 2011; ing and information on the causes and consequences of Kagambèga et al. 2012). foodborne diseases (Barro et al. 2007). The prevalence of Salmonella Tennessee was the most prevalent serotype Salmonella in fish in this study is higher than those re- among fish samples. This serotype of Salmonella was de- ported by Broughton and Walker (2009), from fish in tected in different types of samples and in the stools of China (5%) and by Heinitz et al. (2000) in U.S.-imported patients with diarrhea in other studies from Burkina raw seafood from several Asian countries (10%). These Faso (Kagambèga et al. 2017). Salmonella Tennessee has variations in prevalence can be explained by differences also been implicated in outbreaks in the USA due to in farming methods, and in the food safety regulations of contaminated peanut butter, powdered milk products, each country. For example, in Burkina Faso, many re- and infant formula (Center for Disease Control and Pre- searchers demonstrated that good hygienic practices are vention (CDC) 2007; Center for Disease Control and not respected yet by food sellers and domestic food Prevention (CDC) 1993). These facts show us that the safety regulation and/or training programs are still Tennessee serotype is not necessarily linked to a specific Kagambèga et al. Annals of Microbiology (2021) 71:32 Page 6 of 8 food or environment but can infect humans through important in spreading resistance genes such as bla many contaminated foods. and bla (Xavier et al. 2016). Both strains NDM-1 CTX-M-15 We also have the presence of S. Liverpool and S. did not harbor any beta-lactamase resistance genes. All Teshie, which are pathogenic serotype and have not the Salmonella Liverpool contained Col(pHAD28), been identified in our previous studies carried out in Col4401, and one S. Tennessee possessed Col(MG828) Burkina Faso in diarrheal patients, chickens, the environ- plasmid types. These plasmid types have been associated ment, or animals (Kagambèga et al. 2017; Bonkoungou with quinolone resistances in Salmonella strains (Fiegen et al. 2013; Traoré et al. 2015). Salmonella Derby was et al. 2017). More investigation into these plasmid se- identified as the most dominant in our previous studies quences are needed to determine any benefit they pro- in chickens and slaughter animals (Kagambèga et al. vide the strains. 2013). Salmonella Nima and S. Kokomlemle also have been isolated in chicken and beef previously in Burkina Conclusion Faso (Kagambèga et al. 2013). This study has shown that widely consumed fish in Bur- The presence of these serotypes in fish shows that kina Faso are contaminated with pathogenic bacteria of chicken, slaughter animals, the environment, and the genus Salmonella. The microbiological quality of fish humans share the same pathogens that circulate in our sold in Burkina Faso must be improved to reduce the country. risks of contamination to consumers. Improved food Ten different MLST sequence types were found in this safety will lead to reduced losses, better access to mar- study, and two strains possessed Unknown ST. Two kets, and hence better incomes. The modern molecular MSLT types were detected in our study with S. Tennes- biology technique used in this study, whole-genome se- see. This may show that S. Tennessee has genetic diver- quencing, is a technique that is not yet available in the sity within its population. We can say that the other developing countries. An urgent action is needed by serotype with a unique MSLT type retained their genetic decision-makers in Burkina Faso, other developing coun- characteristic during their evolution while keeping the tries, and countries around the world to collaborate in same type of MLST. On the other hand, S. Tennessee the regulation and monitoring of foodborne pathogens. population structure has changed during evolution. All the Salmonella strains found in this study pos- Abbreviations WGS: Whole-genome sequencing; NTS: Non-typhoidal Salmonella; sessed the aminoglycoside resistance gene encoding ace- CDC: Centers for Disease Control and Prevention; MLST: Multilocus sequence tyltransferases, aac(6′)-Iaa. While this gene was not typing; MDR: Multidrug resistant; LaBESTA: Laboratoire de Biologie functional in the present study and are commonly non- Moléculaire, d’épidémiologie et de surveillance des bactéries et virus transmissible par les aliments; USA: United States of America functional in Salmonella, mutations in the promoter of the gene can lead to expression and phenotypic resist- Acknowledgements ance (Magnet et al. 1999). Rather et al. (1993) demon- We thank the personnel and technicians from the Bacterial Epidemiology strated that aminoglycoside resistance in Salmonella and Antimicrobial Resistance Research Unit, USDA, ARS, Athens, Georgia, USA, for the collaboration and help. strains is usually secondary to increased gene expression following regulatory mutations. Authors’ contributions The fosA7 gene conferring resistance to fosfomycin AK, SB, and SKD carried out the strain’s isolation and characterization. LH, AK, was detected in three antibiotic susceptible strains. Since SP, SKG, HR, and EAM carried out the WGS analysis, AK drafted the manuscript. EAM and LH participated in manuscript writing. NB, CRJ, and JGF this antibiotic was not tested in this study, we cannot supervised the WGS and participated in writing the manuscript. All authors conclude that this gene is functional or not. Rehman read, commented on, and approved of the final manuscript. et al. (2017) demonstrated that the gene fosA7 is respon- sible for fosfomycin resistance. Funding This study was supported by the United States Fulbright scholarship grant to Point mutations in the quinolone resistance- AK and the Bacterial Epidemiology and Antimicrobial Resistance Research determining regions (QRDRs) were detected in 27 (90%) Unit, USDA, ARS, Athens, Georgia, USA. The funding sources had no role in isolates at positions 57 (Thr57Ser), which can confer re- the design of the study and collection, analysis, and interpretation of data and in writing the manuscript. sistance to quinolones. However, all isolates were sus- ceptible to both nalidixic acid and ciprofloxacin. Availability of data and materials Consistent with the results presented here, other Sal- The whole-genome shotgun project has been deposited at GenBank under monella isolates containing this mutation also exhibited BioProject number PRJNA713376 (https://www.ncbi.nlm.nih.gov/bioproject/ susceptibility to nalidixic acid or ciprofloxacin; thus, this PRJNA713376). mutation is thought to not confer resistance in all sero- Declarations types of Salmonella (Baucheron et al. 2005). In this study, two Salmonella Kokomlemle and one S. Ethics approval and consent to participate Teshie possessed IncFII-type plasmids, which have been Not applicable. Kagambèga et al. Annals of Microbiology (2021) 71:32 Page 7 of 8 Consent for publication in Salmonella enterica Serovar Hadar. J Microb Drug Resist 23(3):280–284. 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10.1186/s13213-021-01642-8
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Abstract

Purpose: Fish is an excellent source of protein and vitamins for humans, but improperly handled, fish can expose consumers to pathogenic bacteria. This study was aimed to isolate and characterize the genomes of Salmonella strains isolated from imported fish sold in the open market in Ouagadougou. Methods: One hundred and fifty-nine fish were collected from open markets and were cultured for Salmonella. Antimicrobial susceptibility was determined by broth microdilution. Whole-genome sequencing was done to further study antibiotic resistance genes, plasmid replicons, and MSLT types. Serotyping was done using SeqSero 2. Result: Out of the 159 fish samples analyzed, 30 (18.9%) were found to be contaminated with Salmonella. Among the isolated Salmonella strains, six different serotypes, Nima, Liverpool, Kokomlemle, Teshie, Derby, and Tennessee, were found using SeqSero2. Salmonella Tennessee was the predominant serotype. All the isolates possessed at least one resistance gene. The aac6-Iaa aminoglycoside resistance gene was the most prevalent gene found in the strains. The gene fosA7 was detected in three strains. All the S. Nima isolates were of Multilocus Sequence Type (MLST) 8086, S. Teshie isolate was ST 530; Liverpool was ST 1959; Derby was ST 7880; Kokomlemle was ST 2696. The Tennessee isolates gave two different STs including ST 8395 and 8398. Conclusion: The presented results highlight the prevalence of Salmonella on imported fish purchased from the open markets. More attention should be paid regarding fish selling conditions in the country to prevent the potential health risk for consumers. Keywords: Salmonella, Antimicrobial resistance, Serotype, Fish Introduction has increased exponentially in this country with more Burkina Faso is a landlocked tropical country located than 96% of commercially sold fish imported from in sub-Saharan Africa. This country is characterized another country (Ministry of economic and sustain- by a dry season from October-May with hot able development, Burkina Faso. Statistique doua- temperature (35-45 °C) and a short rainy season nieres 2015). Fish is an important source of essential (June-September). In recent years, fish consumption amino acids and good fatty acids for humans, but fish can be contaminated by pathogenic bacteria that pose * Correspondence: kagambega.asseta@gmail.com; kagamas2007@yahoo.fr a high risk for consumer’s health (Yan et al. 2010; Bacterial Epidemiology and Antimicrobial Resistance Research Unit, U.S. Nwiyi and Onyeabor 2012). These pathogenic bacteria National Poultry Research Center, USDA, ARS, Athens, Georgia, USA Laboratoire de Biologie Moléculaire, d’épidémiologie et de surveillance des can contaminate ready to eat fish product through bactéries et virus transmissibles par les aliments (LaBESTA)/Ecole Doctorale cross-contamination during fish processing (Kris- Sciences et Technologies (EDST), Université Joseph KI-ZERBO, Ouagadougou, Etherton et al. 2002). Burkina Faso Full list of author information is available at the end of the article © The Author(s). 2021 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. Kagambèga et al. Annals of Microbiology (2021) 71:32 Page 2 of 8 Salmonella is a gram-negative foodborne pathogen were placed into a stomacher bag containing 90 mL of and has been implicated in fish outbreaks worldwide buffered peptone water (Liofilchem, Teramo, Italy) and (Barrett et al. 2017; Amagliani et al. 2012). More than homogenized (400 Circulator, Seward, London, UK) for 2500 serotypes of Salmonella have been designated 1 min, then incubated for 24 h at 37 °C. From this non- based on the O and H surface antigens (Issenhuth-Jean- selective pre-enrichment, 0.1 mL were transferred into jean et al. 2014). Several serotypes, including Enteritidis 10 mL of Rappaport-Vassiliadis broth (Oxoid, Basing- and Typhimurium, have been implicated in outbreaks stoke, England) and incubated for 24 h at 42 °C. A loop- associated with seafood sources, though data from Africa ful from the selective enrichment broth was streaked is limited (Amagliani et al. 2012). onto XLD (Oxoid, Basingstoke, England) agar and incu- Currently, the use of antibiotics in aquaculture prac- bated for 24 h at 37 °C. Suspected colonies on selective tices as growth promoters or for treatment and preven- agar plates were purified and bio-typed by using bio- tion of fish diseases is increasing the risk of development chemical tests and API 20E strips (BioMerieux, Marcy of antibiotic resistant bacteria among the microbiome of l’Etoile, France). fish gut and/or fishing water (Miranda et al. 2018). Many Confirmed colonies were sent to the United States De- studies have shown widespread transmission of partment of Agriculture, Agricultural Research Service, antibiotic-resistant bacteria of the fish or aquatic envir- Bacterial Epidemiology and Antimicrobial Resistance Re- onment to humans (Gonzalez-Escalona et al. 2005; search Unit for future analysis. Sørum 2006). According to the Centers for Disease Control and Pre- Antimicrobial susceptibility testing vention (CDC), antibiotic-resistant infection is respon- The isolates were streaked onto Tryptic Soy Agar (TSA) sible for 25,000 annual deaths in the European Union with 5% Sheep blood (BA), (Fisher Scientific, USA) and 23,000 annual deaths in the USA (Center for Dis- plates and incubated for 24 h at 37 °C, and one colony ease Control and Prevention (CDC) 2019). The World from each plate was streaked onto a second BA2 plate Health Organization (WHO) reported that the burden of for another 24 h at 37 °C. Minimum inhibitory concen- food-borne disease is similar to the burden of malaria, trations (MIC, μg/mL) of all Salmonella isolates were tuberculosis, and even HIV/AIDS and is disproportion- determined by broth-microdilution using the Sensititre™ ately borne by the least developed countries and by chil- semi-automated antimicrobial susceptibility system dren (World Health Organization (WHO) 2015). Since (TREK Diagnostic Systems Inc., Cleveland, OH, USA) imported fish is widely consumed in Burkina Faso, it is and the Sensititre™ Gram-Negative plate format, GN4F, important to know the microbiological quality of these (ThermoFisher Scientific, USA), according to manufac- fish. Therefore, the present study aims to understand the turer’s directions. MICs of the isolates for 24 antimicro- epidemiology and antibiotic resistance of Salmonella bials were determined using colonies from the BA2 strains isolated from fish using whole-genome sequen- plates, and each isolate was classified as resistant, inter- cing and phenotypic methods. mediate, or susceptible to the antimicrobials tested using the breakpoints set by Clinical and Laboratory Standards Materials and methods Institute (CLSI) (2016). Antimicrobials used breakpoints −1 Sampling were as follows: Amikacin (≥ 64 μgmL ); Piperacillin/ −1 Imported fish samples were purchased from different tazobactam (≥ 128/4 μgmL ); Tigecycline (≥ 1 μg −1 −1 open markets. All fish samples during collection were mL ); Ticarcillin/clavulanic acid (≥ 128/2 μgmL ); −1 first placed in sterile polypropylene bags, then placed in Levofloxacin (≥ 2 μgmL ); Nitrofurantoin (≥ 128 μg −1 −1 polystyrene boxes containing crushed ice and stored at 4 mL ); Tetracycline (≥ 16 μgmL ); Doripenem (≥ 4 μg −1 −1 °C during transportation. The samples were transported mL ); Minocycline (≥ 16 μgmL ); Ertapenem (≥ 2 μg −1 to the laboratory and processed on the same day for the mL ); Trimethoprim/sulfamethoxazole (≥ 4/76 μg −1 −1 presence of Salmonella spp. mL ); Imipenem (≥ 4 μgmL ); Piperacillin (≥ 128 μg −1 −1 mL ); Meropenem (≥ 4 μgmL ); Gentamicin (≥ 16 μg −1 −1 Bacteriological analysis mL ); Cefazolin (≥ 8 μgmL ); Tobramycin (≥ 16 μg −1 −1 Salmonella strains were isolated from fish samples fol- mL ); Ceftazidime (≥ 16 μgmL ); Ampicillin/sulbac- −1 −1 lowing the methodologies described in the International tam (≥ 32/16 μgmL ); Aztreonam (≥ 16 μgmL ); −1 −1 Organization for Standardization 6579-2017 (Inter- Ampicillin (≥ 32 μgmL ); Cefepime (≥ 32 μgmL ); −1 −1 national Organization for Standardization (ISO) 6579-1 Ciprofloxacin (≥ 4 μgmL ); Ceftriaxone (≥ 4 μgmL ). 2017). The fish samples were gently removed from For the analysis, isolates identified as intermediate were coolers and processed using aseptic conditions. The gills, considered susceptible to the drug. Escherichia coli intestines, and skin were removed using sterile knives. ATCC 25922, Pseudomonas aeruginosa ATCC 27853, About 10 g of samples (fish gills, intestines, and skin) Enterococcus faecalis ATCC 29212, and Staphylococcus Kagambèga et al. Annals of Microbiology (2021) 71:32 Page 3 of 8 aureus ATCC 29213 were controls for determination of and the assembly statistics are shown in Table 1. Among MIC. the isolated Salmonella strains, six different named sero- For each isolate, a final inoculum of 5 × 10 CFU/ml types, including Nima, Liverpool, Kokomlemle, Teshie, was targeted. The panels were read after 18 h of incuba- Derby, and Tennessee were found, with five having no tion at 35 °C. name and only antigenic formulas. Salmonella Tennes- see was the predominant serotype. All the isolates pos- Whole-genome sequencing sessed at least one resistance gene. The non-functional Genomic DNA was isolated using the GenElute bacterial aac6-Iaa conferring resistance to aminoglycosides was genomic DNA kit (Sigma-Aldrich, St. Louis, MO, USA) the most prevalent gene found in the strains. The gene following instructions for Gram-negative bacteria. Cul- fosA7 conferring resistance to Fosfomycin was detected tures were grown in 5 mL of Luria-Bertani Broth, Miller in three strains. The isolates were susceptible to all (Difco™, Becton Dickinson and Company, Sparks, MD) drugs tested using phenotypic method. Four S. Nima overnight at 37 °C with shaking. The extracted DNA isolates were identified from the 30 isolates and were all quality was read using NanoDrop 2000c spectrophotom- MLST Sequence Type (ST) 8086. One S. Teshie isolate eter (Thermo, Fisher Scientific, USA). DNA was stored was identified and was ST 530; three S. Liverpool isolates at −20 °C prior to library preparation. were detected and were identified as ST 1959; one S. Extracted DNA was quantified using the Qubit Derby isolate was found and was ST 7880; one S. double-stranded DNA (dsDNA) high-sensitivity (HS) Kokomlemle was detected and was ST 2696, 15 S. Ten- assay kit according to the manufacturer’s instructions nessee isolates were found, 14 have one of two different (Life Technologies, Inc., USA). The Illumina libraries sequence types, ST 8395 and 8398, and one was un- were prepared using the Nextera XT DNA library prep- known. Plasmid replicon typing results showed six iso- aration kit and Nextera XT index primers (Illumina, lates possessing plasmids: IncFIB and IncFII in the USA). The library fragment size distribution was Teshie isolate, Col(pHAD28) and Col4401 in three Liv- checked using the Bioanalyzer 2100 with an Agilent HS erpool isolates, Col (MG828) in one Tennessee isolate, DNA kit (Agilent Technologies, USA) and quantified and IncFII(S) in one Kokomlemle (Table 2). using a Qubit DNA HS assay kit in a Qubit fluorometer The whole-genome shotgun project has been depos- (Thermo, Fisher Scientific, USA). The generated libraries ited at GenBank under BioProject number were then sequenced using a MiSeq version 2 reagent PRJNA713376 (https://www.ncbi.nlm.nih.gov/bioproject/ kit with 500 or 300 cycles, depending on fragment size. PRJNA713376), and the accession numbers are listed in The paired-end read length of 2 × 250 bp was used for Table 2. The versions described in this paper are the 500 cycles and 2 × 150 bp for 300 cycles on the Illumina first versions. MiSeq platform. The quality metrics of the reads were performed by FastQC (http://www.bioinformatics. Discussion babraham.ac.uk/projects/fastqc/). The sequence data The present study was initiated to determine the micro- were assembled using the A5-miseq assembler (Coil biological quality of imported and local fish consumed et al. 2015), and the genome sequence was annotated via in the city of Ouagadougou, Burkina Faso. The preva- the NCBI Prokaryotic Genome Annotation Pipeline lence of Salmonella strains was 18.9% from imported (Tatusova et al. 2016). fish. This result could be explained by the fact that imported fish are exposed to several stages of handling Identification of antibiotic resistance genes, chromosomal and packaging at the farm in the country of origin, mutations, serotypes, MLST, and plasmid from total transport to Burkina Faso, reception at wholesalers, de- genome sequence livery to semi-wholesalers, and delivery to different re- SeqSero 2 was used to determine the serotypes of Sal- tailers. All these steps undoubtedly favor the monella strains from genome assembly data. Using the contamination by bacteria like Salmonella. However, the Center for Genomic Epidemiology web tools, antibiotic consumption of imported fish is very high in Burkina resistance genes were identified using ResFinder 4.1 Faso because it is very accessible and inexpensive in all (Zankari et al. 2012). MLST sequence type was identified the localities of the country. In these localities, the using MLST 2.0 (Larsen et al. 2012), and plasmids were imported fish is cut into small pieces by small traders detected using PlasmidFinder 2.0 (Carattoli et al. 2014). and sold at a minimum price of 50 FCFA (about one cent of dollar). This necessitates permanent monitoring Results of the prevalence of germs that can affect the health of Out of the 159 fish samples analyzed, 30 (18.9%) were consumers as well as chemicals. The population of Bur- found to be contaminated with Salmonella. From these kina Faso is over 80% illiterate, which will undoubtedly 30 isolates, whole-genome sequences were generated lead to an increase in contamination of raw fish and the Kagambèga et al. Annals of Microbiology (2021) 71:32 Page 4 of 8 Table 1 Assembly statistics of Salmonella strains Isolate Contigs Scaffolds Genome Longest N50 Raw EC % reads Raw nt EC nt % nt Raw EC Median 10th Bases ≥ % ID size scaffold reads reads passing EC passing EC cov cov cov percentile cov Q40 GC 87 61 61 4621725 703602 292745 2075760 2055651 99.03 3.9E+08 3.6E+08 93.77 83.55 78.35 82 59 4617943 52.2 88 61 61 4654102 433362 231906 2480308 2461694 99.25 3.5E+08 3.4E+08 97.2 74.39 72.31 73 54 4651947 52.2 89 180 180 5345366 265739 89976 1585778 1571781 99.12 2.1E+08 2E+08 96.96 39.18 37.99 37 24 5332372 51.8 95 40 40 4680005 668083 504361 2410566 2379641 98.72 4.7E+08 4.4E+08 92.32 100.7 93.01 97 72 4679387 52.2 98 63 63 4918496 775042 398010 1718264 1687773 98.23 3.3E+08 3.1E+08 92.42 67.53 62.41 65 46 4916559 51.9 100 80 80 4963160 748091 287769 2265232 2202986 97.25 4.4E+08 3.9E+08 88.29 89.07 78.65 85 62 4961107 52 101 52 52 4902134 944301 501799 1868462 1821376 97.48 3.8E+08 3.4E+08 90.4 77.46 70.02 74 54 4900597 51.8 103 49 49 4749239 1151741 340547 2323594 2296420 98.83 4.5E+08 4.2E+08 93.23 93.97 87.61 87 63 4748210 52.2 108 44 44 4738594 568197 405801 2091224 2069633 98.97 3.6E+08 3.5E+08 95.15 76.54 72.83 74 55 4737525 52.2 111 47 47 4741632 568232 454680 2514870 2487391 98.91 4.9E+08 4.5E+08 92.81 102.4 95.07 99 76 4740854 52.2 113 49 49 4749008 1444467 340548 2281594 2260595 99.08 4.6E+08 4.3E+08 93.21 97.31 90.7 92 69 4748045 52.2 116 38 38 4661074 871623 424548 1877226 1855294 98.83 3.6E+08 3.3E+08 92.87 76.86 71.37 74 54 4659622 52.2 117 44 44 4739093 568232 427385 2101626 2085634 99.24 3.6E+08 3.5E+08 95.73 76.7 73.42 74 55 4738049 52.2 119 51 51 4730026 508935 323835 1916062 1891245 98.7 2.5E+08 2.4E+08 97.36 52 50.62 50 35 4728141 52.2 122 64 64 4732251 461578 226770 2578950 2550077 98.88 3.4E+08 3.3E+08 96.81 72.58 70.26 71 49 4730117 52.2 127 46 46 4740433 568232 394001 1464044 1447638 98.88 2.6E+08 2.4E+08 95.1 53.95 51.31 52 36 4738090 52.2 128 52 52 4729542 454349 323835 1476660 1454883 98.53 1.9E+08 1.8E+08 97.27 39.56 38.48 38 26 4726471 52.2 129 43 43 4617569 720868 300407 1313142 1295563 98.66 2.4E+08 2.2E+08 93.89 51.58 48.43 50 34 4614768 52.2 130 43 43 4740056 568232 400228 3575342 3520930 98.48 6.6E+08 6E+08 91.2 138.7 126.5 133 101 4739679 52.2 131 53 53 4741832 568232 394156 1566306 1545820 98.69 2.9E+08 2.7E+08 91.49 62.2 56.91 60 42 4739118 52.2 134 34 34 4797111 1850190 750647 2710124 2671347 98.57 5.3E+08 4.8E+08 91.32 110.4 100.8 106 78 4796675 52.2 135 54 54 4903282 944125 424401 2061468 1996430 96.85 3.7E+08 3.3E+08 87.78 75.59 66.35 71 50 4901400 51.8 136 46 46 4747148 857353 340487 1895802 1849828 97.57 3.3E+08 3E+08 90 69.25 62.33 63 43 4745627 52.2 137 44 44 4739464 514012 394016 2219520 2160947 97.36 4.1E+08 3.6E+08 88.01 87.08 76.64 83 60 4738438 52.2 138 42 42 4617148 720868 331382 1581084 1563497 98.89 3.1E+08 2.8E+08 90.95 67.5 61.39 65 46 4615739 52.2 139 45 45 4740410 514012 394637 2120290 2100494 99.07 3.8E+08 3.6E+08 94.39 80.57 76.06 78 56 4739354 52.2 141 71 71 4730418 434837 164778 1976130 1952830 98.82 2.7E+08 2.6E+08 96.44 56.5 54.49 55 39 4726407 52.2 142 45 45 4620013 720868 387756 2282854 2264502 99.2 4.4E+08 4.1E+08 93.92 95.63 89.81 93 68 4619149 52.2 144 688 688 5699254 126378 26527 1655604 1640692 99.1 3.3E+08 3.1E+08 93.14 58.29 54.29 58 27 5652021 51.6 146 385 385 5031347 222688 74906 2781576 2757394 99.13 3.7E+08 3.6E+08 97.48 72.79 70.96 73 46 4988376 52.1 Kagambèga et al. Annals of Microbiology (2021) 71:32 Page 5 of 8 Table 2 Distribution of plasmid replicons and MLSTs of Salmonella from fish Sample ID Serotype Antimicrobial resistances genes Plasmid replicon MLST (ST) ParC mutation Accession numbers 87 Nima aac(6′)-Iaa 0 8086 Thr57Ser SAMN18249072 88 Tennessee aac(6′)-Iaa; fosA7 0 8395 Thr57Ser SAMN18249073 89 Teshie aac(6′)-Iaa IncFIB, IncFII 530 - SAMN18249074 95 Derby aac(6′)-Iaa 0 7880 Thr57Ser SAMN18249075 98 I 39:z10:e,n,z15 aac(6′)-Iaa 0 8401 Thr57Ser SAMN18249076 100 I 30:y:- aac(6′)-Iaa 0 8397 Thr57Ser SAMN18249077 101 I 13:i:z6 aac(6′)-Iaa 0 8396 - SAMN18249078 103 Liverpool aac(6′)-Iaa Col(pHAD28), Col4401 1959 Thr57Ser SAMN18249079 108 Tennessee aac(6′)-Iaa 0 8398 Thr57Ser SAMN18249080 111 Tennessee aac(6′)-Iaa 0 8398 Thr57Ser SAMN16842897 113 Liverpool aac(6′)-Iaa Col(pHAD28), Col4401 1959 Thr57Ser SAMN18249081 116 Tennessee aac(6′)-Iaa; fosA7 0 8395 Thr57Ser SAMN18249082 117 Tennessee aac(6′)-Iaa 0 8398 Thr57Ser SAMN18249083 119 Tennessee aac(6′)-Iaa 0 8398 Thr57Ser SAMN18249084 122 Tennessee aac(6′)-Iaa 0 8398 Thr57Ser SAMN18249085 127 Tennessee aac(6′)-Iaa 0 8398 Thr57Ser SAMN18249086 128 Tennessee aac(6′)-Iaa 0 8398 Thr57Ser SAMN18249087 129 Nima aac(6′)-Iaa 0 8086 Thr57Ser SAMN18249088 130 Tennessee aac(6′)-Iaa 0 8398 Thr57Ser SAMN18249089 131 Tennessee aac(6′)-Iaa Col(MG828) 8398 Thr57Ser SAMN18249090 134 Kokomlemle aac(6′)-Iaa IncFII(S) 2696 Thr57Ser SAMN18249091 135 I 13:i:z6 aac(6′)-Iaa 0 8396 - SAMN18249092 136 Liverpool aac(6′)-Iaa Col(pHAD28), Col4401 1959 Thr57Ser SAMN18249093 137 Tennessee aac(6′)-Iaa 0 8398 Thr57Ser SAMN18249094 138 Nima aac(6′)-Iaa 0 8086 Thr57Ser SAMN18249095 139 Tennessee aac(6′)-Iaa 0 8398 Thr57Ser SAMN18249096 141 Tennessee aac(6′)-Iaa 0 8398 Thr57Ser SAMN18249097 142 Nima aac(6′)-Iaa 0 8086 Thr57Ser SAMN18249098 144 I 39:f,g:e,n,z15 aac(6′)-Iaa 0 Unknown Thr57Ser SAMN18249099 146 Tennessee aac(6′)-laa, fosA7 0 Unknown Thr57Ser SAMN16842913 Less than 100% identity Nearest STs: 384, 696, 1859, 2320, 4924, 5805, 6540, 6730, 6732, 6734 Nearest ST: 8398 possibility of cross-contamination due to a lack of train- missing (Barro et al. 2008; Kagambèga et al. 2011; ing and information on the causes and consequences of Kagambèga et al. 2012). foodborne diseases (Barro et al. 2007). The prevalence of Salmonella Tennessee was the most prevalent serotype Salmonella in fish in this study is higher than those re- among fish samples. This serotype of Salmonella was de- ported by Broughton and Walker (2009), from fish in tected in different types of samples and in the stools of China (5%) and by Heinitz et al. (2000) in U.S.-imported patients with diarrhea in other studies from Burkina raw seafood from several Asian countries (10%). These Faso (Kagambèga et al. 2017). Salmonella Tennessee has variations in prevalence can be explained by differences also been implicated in outbreaks in the USA due to in farming methods, and in the food safety regulations of contaminated peanut butter, powdered milk products, each country. For example, in Burkina Faso, many re- and infant formula (Center for Disease Control and Pre- searchers demonstrated that good hygienic practices are vention (CDC) 2007; Center for Disease Control and not respected yet by food sellers and domestic food Prevention (CDC) 1993). These facts show us that the safety regulation and/or training programs are still Tennessee serotype is not necessarily linked to a specific Kagambèga et al. Annals of Microbiology (2021) 71:32 Page 6 of 8 food or environment but can infect humans through important in spreading resistance genes such as bla many contaminated foods. and bla (Xavier et al. 2016). Both strains NDM-1 CTX-M-15 We also have the presence of S. Liverpool and S. did not harbor any beta-lactamase resistance genes. All Teshie, which are pathogenic serotype and have not the Salmonella Liverpool contained Col(pHAD28), been identified in our previous studies carried out in Col4401, and one S. Tennessee possessed Col(MG828) Burkina Faso in diarrheal patients, chickens, the environ- plasmid types. These plasmid types have been associated ment, or animals (Kagambèga et al. 2017; Bonkoungou with quinolone resistances in Salmonella strains (Fiegen et al. 2013; Traoré et al. 2015). Salmonella Derby was et al. 2017). More investigation into these plasmid se- identified as the most dominant in our previous studies quences are needed to determine any benefit they pro- in chickens and slaughter animals (Kagambèga et al. vide the strains. 2013). Salmonella Nima and S. Kokomlemle also have been isolated in chicken and beef previously in Burkina Conclusion Faso (Kagambèga et al. 2013). This study has shown that widely consumed fish in Bur- The presence of these serotypes in fish shows that kina Faso are contaminated with pathogenic bacteria of chicken, slaughter animals, the environment, and the genus Salmonella. The microbiological quality of fish humans share the same pathogens that circulate in our sold in Burkina Faso must be improved to reduce the country. risks of contamination to consumers. Improved food Ten different MLST sequence types were found in this safety will lead to reduced losses, better access to mar- study, and two strains possessed Unknown ST. Two kets, and hence better incomes. The modern molecular MSLT types were detected in our study with S. Tennes- biology technique used in this study, whole-genome se- see. This may show that S. Tennessee has genetic diver- quencing, is a technique that is not yet available in the sity within its population. We can say that the other developing countries. An urgent action is needed by serotype with a unique MSLT type retained their genetic decision-makers in Burkina Faso, other developing coun- characteristic during their evolution while keeping the tries, and countries around the world to collaborate in same type of MLST. On the other hand, S. Tennessee the regulation and monitoring of foodborne pathogens. population structure has changed during evolution. All the Salmonella strains found in this study pos- Abbreviations WGS: Whole-genome sequencing; NTS: Non-typhoidal Salmonella; sessed the aminoglycoside resistance gene encoding ace- CDC: Centers for Disease Control and Prevention; MLST: Multilocus sequence tyltransferases, aac(6′)-Iaa. While this gene was not typing; MDR: Multidrug resistant; LaBESTA: Laboratoire de Biologie functional in the present study and are commonly non- Moléculaire, d’épidémiologie et de surveillance des bactéries et virus transmissible par les aliments; USA: United States of America functional in Salmonella, mutations in the promoter of the gene can lead to expression and phenotypic resist- Acknowledgements ance (Magnet et al. 1999). Rather et al. (1993) demon- We thank the personnel and technicians from the Bacterial Epidemiology strated that aminoglycoside resistance in Salmonella and Antimicrobial Resistance Research Unit, USDA, ARS, Athens, Georgia, USA, for the collaboration and help. strains is usually secondary to increased gene expression following regulatory mutations. Authors’ contributions The fosA7 gene conferring resistance to fosfomycin AK, SB, and SKD carried out the strain’s isolation and characterization. LH, AK, was detected in three antibiotic susceptible strains. Since SP, SKG, HR, and EAM carried out the WGS analysis, AK drafted the manuscript. EAM and LH participated in manuscript writing. NB, CRJ, and JGF this antibiotic was not tested in this study, we cannot supervised the WGS and participated in writing the manuscript. All authors conclude that this gene is functional or not. Rehman read, commented on, and approved of the final manuscript. et al. (2017) demonstrated that the gene fosA7 is respon- sible for fosfomycin resistance. Funding This study was supported by the United States Fulbright scholarship grant to Point mutations in the quinolone resistance- AK and the Bacterial Epidemiology and Antimicrobial Resistance Research determining regions (QRDRs) were detected in 27 (90%) Unit, USDA, ARS, Athens, Georgia, USA. The funding sources had no role in isolates at positions 57 (Thr57Ser), which can confer re- the design of the study and collection, analysis, and interpretation of data and in writing the manuscript. sistance to quinolones. However, all isolates were sus- ceptible to both nalidixic acid and ciprofloxacin. Availability of data and materials Consistent with the results presented here, other Sal- The whole-genome shotgun project has been deposited at GenBank under monella isolates containing this mutation also exhibited BioProject number PRJNA713376 (https://www.ncbi.nlm.nih.gov/bioproject/ susceptibility to nalidixic acid or ciprofloxacin; thus, this PRJNA713376). mutation is thought to not confer resistance in all sero- Declarations types of Salmonella (Baucheron et al. 2005). In this study, two Salmonella Kokomlemle and one S. Ethics approval and consent to participate Teshie possessed IncFII-type plasmids, which have been Not applicable. Kagambèga et al. Annals of Microbiology (2021) 71:32 Page 7 of 8 Consent for publication in Salmonella enterica Serovar Hadar. J Microb Drug Resist 23(3):280–284. 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Annals of MicrobiologySpringer Journals

Published: Jul 31, 2021

Keywords: Salmonella; Antimicrobial resistance; Serotype; Fish

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