Cross-sectional study to identify risk factors associated with the occurrence of antimicrobial resistance genes in honey bees Apis mellifera) in Umbria, Central Italy


The use antimicrobials for therapeutic and metaphylactic purpose in humans and agriculture exerts selective pressure on animal and environmental microbiota resulting in the survival and spread of antimicrobial resistance genes among bacteria and subsequent development of resistance in bacteria. Previous studies have shown that honey bees’ microbiota (Apis mellifera) can accumulate antimicrobial resistance genes in their microbiome and act as collectors and disseminators of resistance genes. The aim of this study was to investigate to what extent honey bees act as reservoir of select antimicrobial resistance genes. This study was conducted on 35 groups of bees. Bees were collected from 35 sites in Umbria, Italy. PCR was used to screen pooled ground bees’ specimens for genes that code for resistance against antimicrobials that are commonly used in humans and in veterinary medicine including aminoglycosides (aph), beta-lactams (blaZ), tetracycline (tetM) and sulphonamides (sul1 and sul2). Twenty-four samples out of 35 (68.57%) were positive for at least one antimicrobial resistance gene. Two samples were positive for the aph, 5.71%; eight for blaZ, 22.86%; three for tetM, 8.57%; ten for sul1, 28.57% and eighteen for sul2, 51.43%. Positivity to more than one antimicrobial resistance gene was observed in nine samples, 25.71%. The multivariate analysis identified “presence of farms nearby” as the factor most closely related to PCR positivity. Honey bees (Apis mellifera) from Umbria, Italy, carry antimicrobial resistance genes and can be used as indicators of the presence of resistance genes in the environment.

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This work was supported by the Fondazione Cassa Risparmio Perugia, project code 2016.0033.021, Ricerca Scientifica e Tecnologica. The authors wish to express sincere appreciation to members of Polyglot, Perugia, for a careful reading and comments on the manuscript.

Author information

Conceptualization: [B. T. Cenci-Goga, E. Goretti, M. Karama]; Methodology: [L. Grispoldi, P. Sechi]; Formal analysis and investigation: [P. Sechi, R. Ciavarella, M. V. Pipistrelli]; Writing – original draft preparation: [B. T. Cenci-Goga, E. Goretti, M. Karama]; Writing – review and editing: [A. C. Elia, T. Gardi, M. Pallottini, R. Rossi, R. Selvaggi]; Funding acquisition: [B. T. Cenci-Goga, E. Goretti]; Supervision: [B. T. Cenci-Goga, E. Goretti, M. Karama].

Correspondence to Beniamino T. Cenci-Goga.

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• The use of antimicrobials has exerted selective pressure in recent years to determine the onset and spread of antimicrobial resistance genes.

• The use of antimicrobials in humans and animals over time may be associated with the presence of antimicrobial residues in the environment.

• Honey bees (Apis mellifera) are considered an excellent biological indicator of the state of pollution of the territory in which they live thanks to their peculiar characteristics as they can act as collectors and disseminators of antimicrobial resistance genes.

• Honey bees form complex, social networks, the health of which is closely linked to the associated microbial communities living in their gut and can be used as an indicator of the prevalence and distribution of antimicrobial resistance genes in the environment.

• In the study area (region of Umbria, Central Italy), aph, blaZ, tetM, sul1, and sul2 genes are frequent in honey bees’ microbiome, and their prevalence is associated with presence of farms nearby.

Responsible editor: Philippe Garrigues

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Cenci-Goga, B.T., Sechi, P., Karama, M. et al. Cross-sectional study to identify risk factors associated with the occurrence of antimicrobial resistance genes in honey bees Apis mellifera) in Umbria, Central Italy. Environ Sci Pollut Res (2020) doi:10.1007/s11356-020-07629-3

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  • Antimicrobial resistance
  • Honey bees
  • Biological indicator