State of Knowledge on the Acquisition, Diversity, Interspecies Attribution and Spread of Antimicrobial Resistance between Humans, Animals and the Environment: A Systematic Review

Abstract

Resistance to antibiotics is considered one of the most urgent global public health concerns. It has considerable impacts on health and the economy, being responsible for the failure to treat infectious diseases, higher morbidity and mortality rates, and rising health costs. In spite of the joint research efforts between different humans, animals and the environment, the key directions and dynamics of the spread of antimicrobial resistance (AMR) still remain unclear. The aim of this systematic review is to examine the current knowledge of AMR acquisition, diversity and the interspecies spread of disease between humans, animals and the environment. Using a systematic literature review, based on a One Health approach, we examined articles investigating AMR bacteria acquisition, diversity, and the interspecies spread between humans, animals and the environment. Water was the environmental sector most often represented. Samples were derived from 51 defined animal species and/or their products A large majority of studies investigated clinical samples of the human population. A large variety of 15 different bacteria genera in three phyla (Proteobacteria, Firmicutes and Actinobacteria) were investigated. The majority of the publications compared the prevalence of pheno- and/or genotypic antibiotic resistance within the different compartments. There is evidence for a certain host or compartment specificity, regarding the occurrence of ARGs/AMR bacteria. This could indicate the rather limited AMR spread between different compartments. Altogether, there remains a very fragmented and incomplete understanding of AMR acquisition, diversity, and the interspecies spread between humans, animals and the environment. Stringent One Health epidemiological study designs are necessary for elucidating the principal routes and dynamics of the spread of AMR bacteria between humans, animals and the environment. This knowledge is an important prerequisite to develop effective public health measures to tackle the alarming AMR situation.

Keywords: anti-bacterial agent; bacterial; drug resistance; health in social-ecological systems; microbial; one health; resistome.

Figure 1

PRISMA flow diagram of study selection (n¹: H. Meier; n²: K. Spinner).

Figure 2

Number of studies per country (color coded). Grey color means that no studies that fit inclusion criteria were available.

Figure 3

Environmental niches represented in selected studies. “Close animal environment” refers to the holding place of animals. “Close human environment” refers to the household where humans live.

Figure 4

Type of water sources represented by number of included studies (n = 101). “Other water” are other sources than those specified. “Various” sources refer to more than one of those uniquely specified.

Figure 5

Number of studies (y axis) per type of animal sectors (x axis) represented in all 89 studies included. “Animal products” comprised the following: Meat (chicken, turkey, duck, sheep, cattle/beef, fish, pork, offal, not specified), chicken eggs, dairy products (cheese, milk, not specified), and unknown/various. “Livestock birds” comprised the following: Chicken, duck, turkey, goose, ostriches, and other (Hoatzin Cecum). “Fish” compromised the following: Rutilus rutilus, wild eels, salmon, and freshwater fish. “Other” comprised the following: Frog, monkeys, wild boars, peacock, parrot, snake, buffaloes, turtles, red fox, dinoflagellate, dolphin, whales, wolf, other domestic birds, shells, and “other reptiles”.

Figure 6

Type of animal product/food of animal origin represented by included studies.

Figure 7

Human compartment sample types represented by included studies.

Figure 8

Bacteria genera investigated by included studies.

Figure 9

Bacteria phyla represented by included studies.