Insects, Rodents, and Pets as Reservoirs, Vectors, and Sentinels of Antimicrobial Resistance
Abstract
:1. Introduction
2. Antimicrobial Resistance
2.1. Nature
2.2. Mechanisms of AMR
2.3. Conventional and Emerging Analytical Methods for Antimicrobial Resistance
3. The Role of Insects, Rodents, and Pets in AMR Persistence and Transmission
3.1. Insects
3.1.1. How Insects Acquire Resistant Bacteria
3.1.2. Insects as Reservoirs of Antimicrobial Resistance
3.1.3. Insects as Vectors of AMR
3.1.4. Insects as Sentinels of AMR
3.2. Rodents
3.2.1. Rodents as Reservoirs of AMR
3.2.2. Rodents as Vectors of AMR Transmission
3.2.3. Rodents as Sentinels of AMR
3.3. Companion Animals/Pets
3.3.1. Pets as Reservoirs of AMR
3.3.2. Pets as Vectors and Sentinels of AMR
4. Human Exposure and Health Risks
4.1. Human Exposure Pathways
4.2. A Summary of the Inferential Evidence Pointing to Potential Human Health Risks
4.3. Drought on Fertile Grounds? AMR in Insects, Rodents, and Pets in Developing Countries
4.4. Towards a Quantitative Human Health Risk Assessment
5. Human Health Risk Assessment and Mitigation
5.1. Health Risk Assessment
- monitoring the usage of antimicrobial in companion animals,
- the extent to which the AMR occurs in pets, insects, and rodents entering households unintentionally,
- the association between AMR in rodents, insects, and animals of interest, and humans coming in contact with such animals, and
- the routes via which AMR microorganisms and/or ARGs can be transmitted between household animals and humans.
5.2. Mitigation
- limiting the use of antimicrobials in pets only to the clinically justified applications
- raising the awareness of the complex AMR issue within the veterinary specialists and even among the pet owners
- limiting direct contact between pet owners and animals during the use of antimicrobials
- using hand hygiene practices after direct contact with pets
- avoiding intimate contacts with pets through face licking and sharing a bed
- regular cleaning of households; and
- wearing rubber, latex, or vinyl gloves when cleaning urine and droppings from insects, rodents, and pets
- blocking all potential entry routes (foundation cracks, unsealed windows, doors, etc.), particularly in the colder season when the risk of entering is the highest
- sealing garbage bins and containers
- sealing food, including pet foods, to avoid cross-contamination
- cleaning the household to remove uneaten parts of food
- using traps and baits in case of a high risk of infestation; and
- preventing household cats from going outside to limit the predation, potential rodent-cat transmission, and further cat-human transmission.
- collection of dog’s and cat’s droppings and their appropriate disposal to avoid contact with insects (e.g., flies) that feed or develop in excrements, acquisition of AMR and its further spread to humans [95].
- regular cleaning of households
- The use of preventive measures to limit insects from entering the household setting (e.g., screens on windows, mosquito nets); and
- elimination of insects in household setting (e.g., mechanically or chemically in case of infestations)
6. Future Perspectives
6.1. Future Research Directions
6.1.1. Comprehensive Database on AMR in Insects, Rodents, and Companion Animals
6.1.2. Partitioning AMR between Natural and Anthropogenic Pools
6.1.3. Transfer Mechanisms and Behavior in the Environment–Animal–Human Interface
6.1.4. AMR Receptors and Primers in Insects, Rodents, and Companion Animals
6.1.5. Insects as Potential Sources of Novel Antimicrobials to Mitigate AMR
6.1.6. Human Exposure and Health Risks via the Consumption of Edible Insects and Rodents
6.1.7. Quantitative Microbial Risk Assessment
6.1.8. The Contribution of Insects, Rodents, and Pets to the Global Human AMR Burden
6.1.9. Understanding the ‘Human Factor’ in AMR
6.1.10. Increasing the Global Footprint of Developing Regions in AMR Research
6.2. Harnessing Emerging and Novel Tools to Unravel the Complex Behavior of AMR
6.2.1. Genomic Tools
6.2.2. Computational or In-Silico Techniques
6.2.3. Network Analysis
6.2.4. Big Data Analytics
7. Conclusions and Outlook
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
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Insect Name | AMR Organism | AMR Type | ARG Detected | Reference |
---|---|---|---|---|
Houseflies (Musca domestica) Cockroaches (Blattaria/Blattodea) | Enterococci (E. casseliflavus; E. hirae; E. faecium; E. faecalis) | Tetracycline, Erythromycin | Tetracycline tet(M) Erythromycin erm(B) Tn916/1545 transposon family, gelatinase gelE, esp, and asa1 | [37] |
tet(M) and erm(B) and Tn916/1545 transposon family | ||||
Cockroaches (Periplaneta Americana Blattella germanica) | 38 species of gram-negative bacteria, 20 species of glucose non-fermenter bacilli and 6 species of gram-positive bacteria | Ampicillin; Gentamicin; Ciprofloxacin, Ofloxacin; Chloramphenicol Tetracycline; Trimethoprim-sulfamethoxazole; Penicillin; Streptomycin; Erythromycin; Oxacillin; Vancomycin; Cephalothin; Ceftazidime; Imipenem; Piperacillin; Cefoperazone | Not determined | [43] |
Houseflies (Musca domestica) | E. faecalis | Tetracycline; Erythromycin; Streptomycin; Ciprofloxacin; Kanamycin | transposon Tn916 and members of the Tn916/Tn1545 family | [36] |
Houseflies (Musca domestica) | E. coli | Tetracycline; Ampicillin; Streptomycin; Sulfonamides; Trimethoprim-Sulfamethoxazole; Chloramphenicol; Nalidixic acid | Tetracycline tetA and tetB, sulphonamide sul1, sul2, sul3, extended-spectrum b-lactamase blaTEM, strA | [142] |
Stored-product grain insects, e.g., darkling beetle, A. diaperinus; Lesser grain borer, Rhyzopertha dominica; Foreign grain beetle, Ahasverus advena; red flour beetle, Tribolium castaneum (Herbst); warehouse beetle, Trogoderma variabile Ballion; | E. casseliflavus; E. gallinarum; E. faecium; E. faecalis; E. hirae | Tetracycline; Streptomycin; Erythromycin; Kanamycin; Ciprofloxacin; Ampicillin; Chloramphenicol | gelatinase gelE; enterococcal surface protein esp; cytolysin cylA | [143,144] |
Ants (Tapinoma melanocephalum (Fabricius) and Camponotus vittatus (Forel) | Coagulase-positive Staphylococcus (S. aureus); Coagulase-negative Staphylococcus; Gram negative Bacilli | Cephalotine; Oxacillin; Penicillin; Tetracycline; Vancomycin; Ampycillin; Cephalotine; Ciprofloxacine; Sulphazotrin | Not determined | [145] |
Gypsy moth larvae (Lymantria dispar L.) | Enterococcus spp.; members of the Enterobacteriaceae | Carbenicillin; Ceftazidime; Gentamicin; Erythromycin; Kanamycin; Streptomycin; Vancomycin; Chloramphenicol; Rifampin; Nalidixic acid; Tetracycline. | ramA; sdeX; sdeY; blaLRG-1 | [146] |
Bedbugs (Cimex lectularius L.) | E. faecium, S. aureus | Vancomycin; Methicillin; Ampicillin; Teicoplanin; Aminoglycosides Erythromycin | Not determined | [147] |
Honeybees (Apis mellifera L.) | Snodgrassella alvi (Betaproteobacteria) Alphaproteobacteria | Tetracycline Oxytetracyline | tetB, tetC, tetD, tetH, tetL, tetY tetM tetW | [81] |
Houseflies (Musca domestica) False stable flies (Muscina stabulans) | E. coli | Tetracycline; Streptomycin; Kanamycin; Ampicillin; Cefazolin; Cefpodoxime; Trimethoprim | extended-spectrum b-lactamase (ESBL) blaCTX-M-15 | [65] |
Flea midgut (Xenopsylla cheopis) | Yersinia pestis | Streptomycin; Gentamycin; Tetracycline; Chloramphenicol; Sulphonamides | Not determined | [111] |
Houseflies (Musca domestica) blow-flies (Lucilicia species) and Bottle flies (Phaenicia species) | Enterococci (E. casseliflavus; E. gallinarum; E. faecium; E. faecalis) and Staphylococci (S. saprophyticus; S. aureus; S. xylosus; S. epidermidis) | Penicillin, Quinupristin-dalfopristin; Erythromycin; Tetracycline; Clindamycin | erm(B); erm(A); msr(C); msr(A/B); transposon Tn916 | [66] |
Rodent Species | Microbial Species | AMR Profile | Comments | Reference |
---|---|---|---|---|
Rat species 1 | S. aureus, E. coli Pasteurella pnemutropica | Amp (75), Pen (75), AM/Cl (75), Te (12.5) Amp (11.1), Pen (100), Te (25) Amp (11.1), Pen (33.3), AM/Cl (22.2), Te (11.1) | Number in brackets equals % resistance | [176] |
Mice species 1 | S. aureus, E. coli P. pnemutropica | Amp (87.5), Pen (8.5), AM/Cl (37.5), Te (12.5) Pen (8.5) Pen (20) | Number in brackets equals % resistance | [176] |
Rat species 2 | E. coli | Amp (23.3), Strep (15), Tmc (6.6), Te (3.3), Amc (1.7) | Number in brackets equals % resistance | [177] |
Apodemus sylvaticus | E. coli | Amp (48) (21) Tm (33) (8) Cf (21) (4) Ctx (18) (0) | No//in brackets indicate no//of animals with resistant E. coli over no//of animals trapped in coastal vs. inland habitats | [36] |
Rat species 3 | E. coli K. pneumonia Pseudomonus paucimobilis Chryseomonas luteola Aeromonas caviae Burkhoddria cepacia | Te (16.7), Gn (16.7), Apr (16.7), S3 (66.6), C (83.3), Crd (66.6), Cxm (33.3), Amp (50), Na (50), Tm (50) S3 (50), C (100), Crd (100), Amc (100), Cxm (50), Amp (100), Tm (100) Te (12.9), S3 (9.7), C (12.9), Ctx (67.7), Crd (3.2), Amc (9.7), Cxm (16.1), Amp (6.5), Na (41.9), Tm (6.5) Te (15.4), Gn (7.7), Apr (7.7), S3 (23.1), Ctx (92.3), Crd (53.8), Amc (46.2), Cxm (53.8), Amp (4.2), Na (77), Tm (46.2) Te (37.5), Gn (25), S3 (50), Ctx (50), Crd (25), Amc (37.5), Cxm (62.5), Amp (62.5), Na (87.5), Tm (87.5) Te (66.6), Gn (66.6), S3 (66.6), Ctx (66.6), Amc (16.7), Cxm (83.3), Amp (66.6), Na (100), Tm (66.6) | Number in brackets equals % resistance | [178] |
Wild rodents | Hafnia alvei E. coli Serratia liquefaciens | Te (76), Tm (10), Na (24), Ac (98), Ap (95), Cxm (100) Te (14), Na (9), Ac (97), Ap (89), Cxm (100) Te (63), Tm (30), Na (30), Ac (100), Ap (97), Cxm (90) | Number in brackets equals % resistance | [159] |
Wild rodents | Alcaligenes spp. Serratia fonticola Enterobacter intermedius Enterobacter amnigenus Cedacae davisiae Providencia rustigianii | Te (44), Tm (67), Na (56), Ac (67), Ap (67), Cxm (78) Te (50), Na (22), Ac (72), Ap (94), Cxm (67) Te (39), Tm (23), Na (23) Ac (85), Ap (92), Cxm (77) Te (50), Na (40), Ac (90), Ap (100), Cxm (90) Te (44), Tm (22), Na (22), Ac (67), Ap (89), Cxm (89) Te (17), Tm (17), Na (17), Ac (100), Ap (83), Cxm (67) | Number in brackets equals % resistance | [159] |
Rattus rattus, Rattus norvegicus, Mus musculus | E. coli | Amp (35), Te (15), Ap (10), Na (10), C (5), S3 (5), Cf (5), Nf (5) | Number in brackets equals % of isolates showing resistant phenotype | [161] |
Pet | Disease | Causative Bacteria | Reference |
---|---|---|---|
Dogs | Urinary tract infections, | E. coli, Staphylococcus spp. (S. intermedius, S. aureus), P. aeruginosa, E. faecalis, Proteus mirabilis | [202] |
Dental | Actinom-vces spp., Streptococcus spp. and other species | [203] | |
Canine infectious respiratory disease (Kennel Cough) | several viruses/bacteria Streptococcus equi subsp. zooepidemicus Bordetella bronchiseptica Mycoplasma ureaplasma, Mycoplasma acholeplasma, Mycoplasma cynos | [204,205,206] | |
Pasteurellosis | Pasteurella spp. | ||
Bacterial pneumonia | Enterobacteriaceae (e.g., E. coli, Enterobacter spp., Klebsiella spp.), Pasteurella spp., Bordetella bronchiseptica, Streptococcus spp. Clostridium tetani | [204,207] | |
Tetanus (cats) | [208] | ||
Cats Horses | Urinary tract infections Chlamydiosis Tetanus (cats) Strangles Botulism Tetanus (Lockjaw) | Chlamedia felis C. tetani Streptococcus equi Clostridium botulinum C. tetani | [208,209] |
Pet | Resistance | Bacteria | Country | Reference |
---|---|---|---|---|
Dogs, Cats | Ampicillin (18%) | E. coli | Belgium, Italy, Netherlands | [24] |
Dogs | Imipenem (0.2%), colistin (5%) | K. pneumoniae | Portugal | [218] |
Methicillin | S. aureus | [209] | ||
Dogs, cats | Cefotaxime (66–75%) Ceftazidime (71–80%) | E. coli | Italy | [197] |
Dogs | Cefazolin (43%), fluoroquinolone (22%) | E. coli | Taiwan | [219] |
Dogs, Cats | chloramphenicol, tetracycline, doxycycline, co-trimoxazole, ampicillin, cefotaxime | Klebsiella spp. | India | [198] |
amoxicillin (4.8%), ampicillin (21.2%), lincomycin (98%), tetracycline (95%)_enrofloxacine(77%), ofloxacin (64%), ciprofloxacin (73%) | Enterococcus spp. (E. faecium, E. avium, E. faecalis) | Portugal | [196] | |
Dogs, Cats | Methicillin | Staphylococcus pseudintermedius (63%), S. aureus (50%) | Singapore | [220] |
Fluoroquinolone | E. coli (40%) | [220] | ||
Carbapenem | K. pneumoniae (7%) | [220] | ||
Cats | Ampicillin (42%), amoxicillin/clavulanate (53%), erythromycin 40%), tetracycline (24%), ciprofloxacin (63%), teicoplanin, vancomycin (24%) | E. faecium, E. faecalis | Italy | [197] |
Horses | Cephalosporin, ciprofloxacin Gentamycin, tobramycin | K. pneumoniae | Austria | [199] |
Horses | Several antibiotics | E. coli | USA | [221] |
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Gwenzi, W.; Chaukura, N.; Muisa-Zikali, N.; Teta, C.; Musvuugwa, T.; Rzymski, P.; Abia, A.L.K. Insects, Rodents, and Pets as Reservoirs, Vectors, and Sentinels of Antimicrobial Resistance. Antibiotics 2021, 10, 68. https://doi.org/10.3390/antibiotics10010068
Gwenzi W, Chaukura N, Muisa-Zikali N, Teta C, Musvuugwa T, Rzymski P, Abia ALK. Insects, Rodents, and Pets as Reservoirs, Vectors, and Sentinels of Antimicrobial Resistance. Antibiotics. 2021; 10(1):68. https://doi.org/10.3390/antibiotics10010068
Chicago/Turabian StyleGwenzi, Willis, Nhamo Chaukura, Norah Muisa-Zikali, Charles Teta, Tendai Musvuugwa, Piotr Rzymski, and Akebe Luther King Abia. 2021. "Insects, Rodents, and Pets as Reservoirs, Vectors, and Sentinels of Antimicrobial Resistance" Antibiotics 10, no. 1: 68. https://doi.org/10.3390/antibiotics10010068
APA StyleGwenzi, W., Chaukura, N., Muisa-Zikali, N., Teta, C., Musvuugwa, T., Rzymski, P., & Abia, A. L. K. (2021). Insects, Rodents, and Pets as Reservoirs, Vectors, and Sentinels of Antimicrobial Resistance. Antibiotics, 10(1), 68. https://doi.org/10.3390/antibiotics10010068