View More View Less
  • 1 University of Lagos, Nigeria
  • 2 Nigerian Institute of Medical Research, Nigeria
  • 3 Centre Nationale de Référence de Salmonella, France
  • 4 Lagos University Teaching Hospital, Nigeria
Restricted access

Purchase article

USD  $25.00

1 year subscription (Individual Only)

USD  $784.00

Outbreaks of Salmonellosis remain a major public health problem globally. This study determined the diversity and antibiotic resistance gene profile of Salmonella enterica serovars isolated from humans and food animals. Using standard methods, Salmonella spp. were isolated from fecal samples, profiled for antimicrobial susceptibility and resistance genes. Seventy-one Salmonella isolates were recovered from both humans and food animals comprising cattle, sheep, and chicken. Forty-four serovars were identified, with dominant Salmonella Budapest (31.8%). Rare serovars were present in chicken (S. Alfort, S. Wichita, S. Linton, S. Ealing, and S. Ebrie) and humans (S. Mowanjum, S. Huettwillen, S. Limete, and S. Chagoua). Sixty-eight percent of isolates were sensitive to all test antibiotics, while the highest rate of resistance was to nalidixic acid (16.9%; n = 12), followed by ciprofloxacin (11.3%; n = 8) and tetracycline (9.9%; n = 8). Five isolates (7%) were multidrug-resistant and antimicrobial resistance genes coding resistance to tetracycline (tetA), beta-lactam (blaTEM), and quinolone/fluoroquinolone (qnrB and qnrS) were detected. Evolutionary analysis of gyrA gene sequences of human and food animal Salmonella isolates revealed variations but are evolutionarily interconnected. Isolates were grouped into four clades with S. Budapest isolate from cattle clustering with S. Budapest isolated from chicken, whereas S. Essen isolated from sheep and chicken was grouped into a clade. Diverse S. enterica serovars with high antibiotic resistance profile are ubiquitous in food animals; hence, there is a need for surveillance and prudent use of antibiotics in human and veterinary medicine.

  • 1.

    Crump, J. A., Sjolund-Karlsson, M., Gordon, M. A., Parry, C. M.: Epidemiology, clinical presentation, laboratory diagnosis, antimicrobial resistance and antimicrobial management of invasive Salmonella infections. Clin Microbiol Rev 28, 901937 (2015).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 2.

    Freitas, N. O. C., Penha, F. R. A. C., Barrow, P., Berchier, J. A.: Source of human non-typhoidal salmonellosis: A review. Braz J Poultry Sci 12, 111 (2010).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 3.

    Mellon, G., Delanoe, C., Roux, A. L., Heym, B., Dubourg, O., Hardy, P., Chevallier, B., Perronne, C., Rouveix, E., Salomon, J.: Non-typhi Salmonella enterica urinary tract infection. Med Mal Infect 47, 389393.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 4.

    Marks, F., von Kalckrevth, V., Aaby, P., Adu-Sarkodie, Y., El-Tayeb, M. A., Ali, M., Aseffa, A., Baker, S., Biggs, H. M., Bjerregaard-Andersen, M., Breiman, R. F., Campbell, J. I., Cosmas, L., Crump, J. A., Espinoza, L. M., Deerin, J. F., Dekker, D. M., Fields, B. S., Gasmelseed, N., Hertz, J. T., Van Minh Hoang, N., Im, J., Jaeger, A., Jeon, H. J., Kabore, L. P., Keddy, K. H., Konings, F., Krumkamp, R., Ley, B., Løfberg, S. V., May, J., Meyer, C. G., Mintz, E. D., Montgomery, J. M., Niang, A. A., Nichols, C., Olack, B., Pak, G. D., Panzner, U., Park, J. K., Park, S. E., Rabezanahary, H., Rakotozandrindrainy, R., Raminosoa, T. M., Razafindrabe, T. J., Sampo, E., Schütt-Gerowitt, H., Sow, A. G., Sarpong, N., Seo, H. J., Sooka, A., Soura, A. B., Tall, A., Teferi, M., Thriemer, K., Warren, M. R., Yeshitela, B., Clemens, J. D., Wierzba, T. F.: Incidence of invasive Salmonella disease in Sub-Saharan Africa: A multicenter population based surveillance study. Lancet Glob Health 5, e310323 (2017).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 5.

    Deekshit, V. K., Kumar, B. K., Rai, P., Rohit, A., Karunasagar, I.: Simultaneous detection of Salmonella pathogenicity island 2 and its antibiotic resistance genes from seafood. J Microbiol Methods 93, 233238 (2013).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 6.

    Smith, S., Branu, S., Akintimehin, F., Fesobi, T., Bamidele, M., Coker, A., Monecke, S., Ehricht, R.: Serogenotyping and antimicrobial susceptibility testing of Salmonella spp. isolated from retail meat samples in Lagos, Nigeria. Mol Cell Probe 30, 189194 (2016).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 7.

    Kjeldsen, M. K., Torpdah, I. M., Campos, J., Pedersen, K., Nielsen, E. M.: Multiple locus variable number tandem repeat analysis of Salmonella enterica subsp. enterica serovar Dublin. J Appl Microbiol 116, 10441054 (2014).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 8.

    Raufu, I. A., Lawan, F. A., Bello, H. S., Musa, A. S., Ameh, J. A., Ambali, A. G.: Occurrence and antimicrobial susceptibility profiles of Salmonella serovars from fish in Maiduguri Sub-Saharan Nigeria. Egypt J Aquat Res 40, 5963 (2014).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 9.

    Niemann, J., Tietze, E., Ruddat, I., Fruth, A., Prager, R., Rabsch, W., Blaha, T., Munchhausen, C., Merle, R., Kreienbrock, L.: Epidemiological analysis of the dynamic and diversity of Salmonella spp. in five German pig production clusters using phenol and genotyping methods: An exploratory study. Vet Microbiol 176, 190195 (2015).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 10.

    Aboud, O. A. A., Adaska, J. M., Williams, D. R., Rossitto, P. V., Champagne, J. D., Lehenbauer, T. W., Atwill, R., Li, X., Aly, S. S.: Epidemiology of Salmonella sp. in California cull dairy cattle: Prevalence of faecal shedding and diagnostic accuracy of pooled enriched broth culture of faecal samples. Peer J 4, e2386 (2016).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 11.

    Fagbamila, I. O., Barco, L., Mancin, M., Kwaga, J., Ngulukun, S. S., Zavagnin, P.: Salmonella serovars and their distribution in Nigeria commercial chicken layer farms. PLoS One 12, e0173097 (2017).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 12.

    Yue, M., Schifferli, D. M.: Allelic variation in Salmonella: An underappreciated driver of adaptation and virulence. Front Microbiol 4, 419 (2014).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 13.

    World Health Organization. Antimicrobial Resistance. Global Report on Surveillance. Geneva, Switzerland: WHO Press, World Health Organization, 2014. Available at www.who.int

    • Search Google Scholar
    • Export Citation
  • 14.

    Abatcha, M. G., Zakaria, Z., Kaur, D. G., Thong, K. L.: Review article: A trend of Salmonella and antibiotic resistance. Adv Life Sci Technol 17, 921 (2014).

    • Search Google Scholar
    • Export Citation
  • 15.

    Yi, L., Wang, J., Gao, Y., Liu, Y., Doi, Y., Wu, R., Zeng, Z., Liang, Z., Liu, J.-H.: MCr-1- Harboring Salmonella enterica serovar Typhimurium sequence type 34 in pigs, China. Emerg Infect Dis 23, 291295 (2017).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 16.

    Djeffal, S., Bakour, S., Mamache, B., Elgroud, R., Agabou, A., Chabou, S., Hireche, S., Bouaziz, O., Rahal, K., Rolain, J. M.: Prevalence and clonal relationship of ESBL-producing Salmonella strains from humans and poultry in Northeastern Algeria. BMC Vet Res 13, 132 (2017).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 17.

    Fashae, K., Ogunsola, F., Aarestrup, F. M., Hendriksen, R. S.: Antimicrobial susceptibility and serovars of Salmonella from chicken and humans in Ibadan, Nigeria. J Infect Dev Ctries 4, 484494 (2010).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 18.

    Smith, S. I., Fowora, M. A., Goodluck, H. A., Nwaokorie, F. O., Aboaba, O. O., Opere, B.: Molecular typing of Salmonella spp. isolated from food handlers and animals in Nigeria. Int J Mol Epidemiol Genet 2, 7377 (2011).

    • Search Google Scholar
    • Export Citation
  • 19.

    Agada, G. O. A., Abdullahi, I. O., Aminu, M., Odugbo, M., Chollom, S. C., Kumbish, P. R., Okwori, A. E. J.: Prevalence and antibiotic resistance profile of Salmonella isolates from commercial poultry and poultry farm-handlers in Jos, Plateau state Nigeria. Br Microbiol Res J 4, 462479 (2014).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 20.

    Smith, S. I., Fowora, M. A., Tiba, A., Anejo-Okopi, J., Fingesi, T., Adamu, M. E., Omonigbehin, E. A., Ugo-IJeh, M. I., Bamidele, M., Odeigah, P.: Molecular detection of some virulence genes in Salmonella spp. isolated from food samples in Lagos, Nigeria. Anim Vet Sci 3, 2227 (2015).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 21.

    Grimont, P. A. D., Weill, F. X.: Antigenic Formulae of the Salmonella Serovas, 9th Edition. World Health Organization Collaborating Center for Reference and Research on Salmonella Institute Pasteur, Paris, France, 2007.

    • Search Google Scholar
    • Export Citation
  • 22.

    The European Committee on Antimicrobial Susceptibility Testing (EUCAST): Break Point Tables for Interpretation of MICs and Zone Diameters Version 1.0, 2016. Available at http://www.eucast.org (Accessed 16 April 2017).

    • Search Google Scholar
    • Export Citation
  • 23.

    Adi, P. J., Naidu, J. R., Matcha, B.: Multiplex quantification of Escherichia coli, Salmonella typhi and Vibrio cholera with three DNA targets in single reaction assay. Microb Pathog 110, 5055 (2017).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 24.

    Cavaco, L. M., Frimodt-Moller, N., Hasman, H., Guardabassi, L., Nielsen, L., Aarestrup, F. M.: Prevalence of quinolone resistance mechanisms and associations to minimum inhibitory concentrations in quinolone-resistant Escherichia coli isolated from humans and swine in Denmark. Microb Drug Resist 14, 163169 (2008).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 25.

    Cattoir, V., Weill, F. X., Poirel, L., Fabre, L., Soussy, C. J., Nordmann, P.: Prevalence of qnr genes in Salmonella in France. J Antimicrob Chemother 59, 751754 (2007).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 26.

    Wiuff, C., Madsen, M., Baggesen, D. L., Aarestrup, F. M.: Quinolone resistance among Salmonella enterica from cattle broilers, and swine in Denmark. Microb Drug Resist 6, 1117 (2000).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 27.

    Olesen, I., Hasman, H., Aarestrup, F. M.: Prevalence of beta-lactamases among ampicillin-resistant Escherichia coli and Salmonella isolated from food animals in Denmark. Microb Drug Resist 10, 334340 (2004).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 28.

    Hendriksen, R. S., Mikoleit, M., Kornschober, C., Rickert, R. L., Duyne, S. V., Kjelso, C., Hasman, H., Cormican, M., Mevius, D., Threlfall, J., Angulo, F. J., Aarestrup, F. M.: Emergence of multidrug resistant Salmonella Concord infection in Europe and the United States in children adopted from Ethiopia 2003–2007. Pediatr Infect Dis J 28, 814818 (2009).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 29.

    Arlet, G., Rouveau, M., Philippon, A.: Substitution of alanine for aspartate at position 197 in the SHV-6 extended spectrum beta-lactamase. FEMS Microbiol Lett 152, 163167 (2007).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 30.

    Waters, S. H., Rogowsky, P., Grinsted, J., Altenbuchner, J., Schmitt, R.: The tetracycline resistance determinants of RP1 and Tn1721: nucleotide sequence analysis. Nucleic Acids Res 11, 60896105 (1983).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 31.

    Sengelov, G., Agerso, Y., Halling-Sorensen, B., Baloda, S. B., Andersen, J. S., Jensen, L. B.: Bacterial antibiotic resistance levels in Danish farmland as a result of treatment with pig manure slurry. Environ Int 28, 587595 (2003).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 32.

    Kumar, S., Stecher, G., Tamura, K.: MEGA 7: Molecular Evolutionary Genetic Analysis version 7.0 for bigger datasets. Mol Biol Evol 33, 18701874 (2016).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 33.

    Raufu, I., Hendriksen, R. S., Ameh, J. A., Aarestrup, F. M.: Occurrence and characterization of Salmonella Hiduddify from chicken and poultry meat in Nigeria. Foodborne Pathog Dis 6, 425430 (2009).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 34.

    Centers for Disease Control and Prevention (CDC): National Salmonella Surveillance Annual Report, 2013. Atlanta, Georgia: US Department of Health and Human Services, CDC, 2016. Available at www.cdc.gov/nationalsurveillance/Salmonella-surveillance.html.Accessed on: September 20, 2017).

    • Search Google Scholar
    • Export Citation
  • 35.

    Morpeth, S. C., Ramadhani, H. O., Crump, J. A.: Invasive non-Typhi Salmonella disease in Africa. Clin Infect Dis 49, 606611 (2009).

  • 36.

    Mezal, E. H., Stefanova, R., Khan, A. A.: Isolation and molecular characterization of Salmonella enterica serovar Javiana from food, environment and clinical samples. Int J Food Microbiol 164, 113118 (2013).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 37.

    Medalla, F., Gu, W., Mahon, B. E., Judd, M., Folster, J., Griffin, P. M., Hoekstra, R. M.: Estimated incidence of antimicrobial drug-resistant nontyphoidal Salmonella infections, United States, 2004–2012. Emerg Infect Dis 23, 2937 (2017).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 38.

    Boqvist, B. S., Hansson, I., Bjerselius, U. N., Hamilton, C., Wahlstrom, H., Noll, B., Tysen, E., Engvau, A.: Salmonella isolated from animals and feed production in Sweden between 1993–1997. Acta Vet Scand 44, 181197 (2003).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 39.

    Trongjit, S., Angkititrakul, S., Tuttle, R. E., Poungseree, J., Padungtod, P., Chuanchuen, R.: Prevalence and antimicrobial resistance in Salmonella enterica isolated from broiler chicken, pigs and meat products in Thailand-Cambodia border provinces. Microbiol Immunol 61, 2333 (2017).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 40.

    Wen, S. C. H., Best, E., Nourse, C.: Non-typhoidal Salmonella infections in children: Review of literature and recommendations for management. J Paediatr Child Health 53, 936941 (2017).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 41.

    Raufu, I., Bortolaia, V., Svendsen, C. A., Ameh, J. A., Ambali, A. G., Aarestrup, F. M., Hendriksen, R. S.: The first attempt of an active integrated laboratory based Salmonella surveillance programme in the north-eastern region of Nigeria. J Appl Microbiol 115, 10591067 (2013).

    • Search Google Scholar
    • Export Citation
  • 42.

    Zhu, Y., Lai, H., Zou, L., Yin, S., Wang, C., Han, X., Xia, X., Hu, K., He, L., Zhou, K., Chen, S., Ao, X., Liu, S.: Antimicrobial resistance and resistance genes in Salmonella strains isolated from broiler chickens along the slaughtering process in China. Int J Food Microbiol 259, 4351 (2017).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 43.

    Afzal, A., Sarwar, Y., Ali, A., Maqbool, A., Salman, M., Habeeb, M. A., Haque, A.: Molecular evaluation of drug resistance in clinical isolates of Salmonella enterica serovar Typhi from Pakistan. J Infect Dev Ctries 7, 929940 (2013).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 44.

    Adesiji, Y. O., Deekshit, V. K., Karunasagar, I.: Antimicrobial-resistant genes associated with Salmonella spp. isolated from human, poultry and seafood sources. Food Nutr 2, 436442 (2014).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 45.

    Fashae, K., Hendriksen, R. S.: Diversity and antimicrobial susceptibility of Salmonella enterica serovars isolated from pig farms in Ibadan, Nigeria. Folia Microbiol 59, 6977 (2013).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 46.

    Tadesse, G., Tessema, T. S., Beyene, G., Aseffa, A.: Molecular epidemiology of fluoroquinolone resistant Salmonella in Africa: A systematic review and meta-analysis. PLoS ONE 13, e0192575 (2018).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 47.

    Baker, S., Duy, P. T., Nga, T. V. T., Dung, T. T. N., Phat, V. V., Chau, T. T., Turner, A. K., Farrar, J., Boni, M. F.: Fitness benefits in fluoroquinolone resistant Salmonella Typhi in the absence of antimicrobial pressure. eLife 2, e01229 (2013).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 48.

    Griggs, D. J., Gensberg, K., Piddock, L. J. V.: Mutations in gyrA gene of quinolone resistant Salmonella serotypes isolated from humans and animals. Antimicrob Agents Chemother 40, 10091013 (1996).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 49.

    Chattaway, M. A., Aboderin, A. O., Fashae, K., Okoro, C. K., Opintan, J. A., Okeke, I. N.: Fluoroquinolone-resistant enteric bacteria in sub-Saharan Africa: Clones, implications and research needs. Front Microbiol 7, 558 (2016).

    • Crossref
    • Search Google Scholar
    • Export Citation

Monthly Content Usage

Abstract Views Full Text Views PDF Downloads
Sep 2020 50 5 1
Oct 2020 83 0 0
Nov 2020 30 4 1
Dec 2020 16 0 0
Jan 2021 13 0 0
Feb 2021 30 0 0
Mar 2021 2 0 0