Next Article in Journal
The Protective Effect against Lung Injury of Phytosome Containing the Extract of Purple Waxy Corn Tassel in an Animal Model of PM2.5-Induced Lung Inflammation
Previous Article in Journal
Optimization and Preparation of Ultrasound-Treated Whey Protein Isolate Pickering Emulsions
 
 
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Perspective

Antibiotic Resistance Genes in Global Food Transformation System: Edible Insects vs. Livestock

State Key Laboratory of Resource Insects, Institute of Apicultural Research, Chinese Academy of Agricultural Sciences, Beijing 100093, China
*
Author to whom correspondence should be addressed.
These authors contributed equally to this work.
Foods 2024, 13(20), 3257; https://doi.org/10.3390/foods13203257
Submission received: 10 September 2024 / Revised: 10 October 2024 / Accepted: 11 October 2024 / Published: 13 October 2024
(This article belongs to the Section Food Security and Sustainability)

Abstract

:
Antibiotic-resistant genes (ARGs) pose a significant threat to the global food transformation system. The increasing prevalence of ARGs in food has elicited apprehension about public health safety. The widespread dissemination of ARGs in food products, driven by the inappropriate use of antibiotics, presents significant adversity for the safety of emerging future food sources such as edible insects. As the world faces increasing challenges related to food security, climate change, and antibiotic resistance, edible insects offer a sustainable and resilient food source. The intriguing possibility of edible insects serving as a less conducive environment for ARGs compared to livestock warrants further exploration and investigation. In this recent work, we listed ARGs from edible insects detected so far by in vitro approaches and aimed to construct a fair comparison with ARGs from livestock based on relevant genes. We also presented our argument by analyzing the factors that might be responsible for ARG abundance in livestock vs. edible insects. Livestock and edible insects have diverse gut microbiota, and their diets differ with antibiotics. Consequently, their ARG abundance may vary as well. In addition, processed edible insects have lower levels of ARGs than raw ones. We hypothesize that edible insects could potentially contain a lower abundance of ARGs and exhibit a diminished ability to disseminate ARGs relative to livestock. A regulatory framework could help intercept the increasing prevalence of ARGs. Due diligence should also be taken when marketing edible insects for consumption.

1. Introduction

Antibiotic resistance (AR) has been defined as the “quintessential” health concern. Due to the overuse of antibiotics in agriculture, the food industry, and pharmaceuticals, the issue is growing serious day by day, leading to an increase in drug-resistant infections in humans and animals. The antibiotic-resistant genes (ARGs) responsible for causing these infections are prevalent and diverse in environments where AR selection and transmission occur regularly. ARGs can spread through bacteria in livestock, dairy, shellfish, and other food sources. They reach animals via surface, groundwater, soil, and air [1]. AR poses a significant threat to public health, resulting in approximately 4.95 million deaths worldwide and 1.3 million fatalities annually in China alone [2,3]. Due to the lack of new antibiotics development, it is crucial to practice antibiotic stewardship immediately.
Foods are quite vulnerable to ARG propagation. Novel food substitutes like edible insects are not out of this spectrum. Edible insects are emerging as a promising global food transformation system component. Their high nutritional value and relatively low environmental impact make them a compelling alternative to traditional livestock. According to nutritional data, edible insects are a promising source of micronutrients (copper, zinc, manganese, phosphorus, selenium, riboflavin, pantothenic acid, biotin, and folic acid) as well as proteins [2,3,4]. Furthermore, research has demonstrated that edible insect fiber, chitin, and omega-3 fatty acids are beneficial for both human and animal gut bacteria [5]. Insect-based food has a long history in Southeast Asia, and insects like crickets, grasshoppers, and mealworms are commonly consumed in tropical and subtropical regions. While insects are not yet widely consumed in other parts of the world, their acceptance and integration into traditional cuisines are on the rise [4,6]. Out of 2000 edible insect species, the European Union has authorized four so far in frozen, dried, and powdered form: Tenebrio molitor larvae, Locusta migratoria, Acheta domesticus, and Alphitobius diaperinus. By incorporating insects into our diets, we can diversify our food systems, reduce our reliance on resource-intensive animal agriculture, and contribute to a more sustainable future. Therefore, determining the risk factor for edible insects is becoming crucial. The risk of using insects as food ingredients or in food product manufacturing is unclear [7]. In terms of microbiological risks, insects can carry bacteria species in their gut and cuticle. They can also be a source of transferable ARGs that are associated with edible insects and opportunistic human pathogens [8,9]. However, while the use of antibiotics in livestock is a major contributor to ARGs, edible insects typically use fewer antibiotics, reducing the likelihood of breeding resistant strains [10,11]. Moreover, the comparative simplicity of insect microbiomes compared to those of farm animals may impede the transfer of antimicrobial resistance genes [12,13].
We hypothesized that the abundance of ARGs in insects could be lower than in animals because of the differences in their diet, microbial diversity, and farming process. Given the frequency and transmission of ARGs, edible insects may be less threatening than animals. Additionally, appropriate processing may assist in mitigating ARGs by minimizing the microbial load in edible insects.

2. Prevalent ARGs in Insects and Livestock

Only a handful of studies revealed a widespread prevalence of genes in edible insects that confer resistance to different antibiotics. Nonetheless, the extent of human exposure to ARGs carried by market-available edible insects is far from being determined, let alone the wild-reared ones (Table 1). ARGs in livestock, however, have been the subject of substantial research. When comparing the prevalence of ARGs between edible insects and livestock, a complex narrative emerges, highlighting the diverse microbial landscapes in these food sources (Figure 1).
While both edible insects and livestock harbor ARGs, their distribution and prevalence vary significantly. For instance, edible insects exhibit a notable prevalence of tet genes, while livestock demonstrates a higher abundance of tet and erm genes, along with several bla gene strains. Addressing AR in food sources requires a holistic understanding of microbial ecology and targeted interventions to promote sustainable farming practices and safeguard public health.
Edible insects exhibit a notable prevalence of certain ARGs, such as tet(K), tet(M), and tet(S). Studies by Milanovic and colleagues underscore the widespread occurrence of these genes in edible insects, with high positivity rates observed in samples collected from Thailand and the Netherlands. Tet(K) demonstrated the highest prevalence, with 90.9% positivity among 11 samples from those regions, followed by tet(S) with 54.5% positivity [8]. Similarly, ready-to-eat grasshoppers and mealworms from various regions of Europe displayed a high distribution of tet(M), tet(K), and tet(S), indicating a consistent pattern across different insect species and geographical locations [17,19]. Conversely, livestock, particularly in Europe and selected Asian regions, demonstrate a higher prevalence of genes like tet(W), tet(A), tet(B), and tet(M). Research by Yang et al. and Jalencu elucidates the dominance of these genes in pig and duck farms, emphasizing their widespread presence within conventional livestock production systems [21,22].
In addition to the tet genes, the prevalence of erm(B) and erm(C) in both edible insects and livestock is worth noting. While these genes are less frequent in edible insects compared to tet genes, they still exhibit a significant presence, particularly in European insect species and livestock populations. For example, Milanovic et al., in 2016, found 45.4% and 18.2% of edible insect samples from the Netherlands and Thailand were positive for erm(B) and erm(C), respectively [8]. In 2017, Osimani and his team found consistent prevalence for erm(B) and erm (C) in ready-to-eat grasshoppers from the Netherlands, Thailand, and Belgium [23]. Erm(B) was the most abundant (57.5%) in France and Thailand, while no positivity was found in Belgium and the Netherlands [16]. Erm(B) is the most abundant in European livestock, followed by Erm(C). In several animal farms in northern and southern China, erm(B) and erm(C) were found to be abundant [24,25]. In a study of pig farms in 25 Thai provinces, Erm(B) was also found to be resistant to primary microlide [26]. The consistency of these findings across different studies underscores the importance of understanding the broader microbial ecology of food sources to mitigate the spread of antibiotic resistance.
However, it is essential to acknowledge that the prevalence of the bla gene strains appeared somewhat higher in livestock than in edible insects. Studies by Milanovic et al. and Osimani et al. reveal a comparatively lower occurrence of blaZ and mecA in edible insects from Europe and Thailand, suggesting potential differences in the mechanisms of antibiotic resistance between both protein sources [8,15,20]. Furthermore, the prevalence of extended-spectrum β-lactamase (ESBL) genes, e.g., blatem blactx-m, and blashv in livestock, particularly in chicken meat, highlights the need for targeted interventions to address antibiotic resistance in conventional livestock farming [27].
Although vancomycin resistance and aminoglycosides are rarely seen in livestock or edible insects, recent research by Osimani et al. shows that ready-to-eat mealworms and grasshoppers from the European market have a low frequency of aac-aph [17,23]. Vancomycin-resistant genes vanA and vanB have also been reported occasionally in both dietary sources. Aac(3)-Iia, aac(6′)-Ib, and aph(3′)-IIIa have all been found in cattle, chicken, and swine in Europe, South Korea, and China, even though utilizing aminoglycosides in livestock is discouraged due to potentially dangerous residues [28,29,30,31]. It is interesting to note that van(A) is the most common vancomycin-resistant gene in cattle; however, it is not that common compared to other ARGs.
This comparative analysis of ARG prevalence in edible insects and livestock reveals a nuanced landscape, with distinct patterns emerging across different gene families and animal sources.
Unfortunately, there is a huge gap in research regarding ARGs in edible insects. Studies are restricted to PCR methods with gut-specific samples of edible insects, whereas studies on livestock have concentrated on metagenomics and waste samples. It remains unavoidable, however, that ARGs might be more common in livestock than edible insects.

3. Probable Reasons for ARG Abundance: Edible Insects vs. Livestock

Addressing AR in food sources requires a holistic understanding of microbial ecology and targeted interventions to promote sustainable farming practices and safeguard public health. The gut microbiome is the primary determinant of the abundance of ARGs in edible insects and animals. The consumption of antibiotics and diets are important factors as well. Environmental factors like pollution and waste production can also contribute to the abundance of ARGs in edible insects and livestock.

3.1. Gut Microbiome

Insects can support a diverse autochthonous microbial community of viruses, fungi, bacteria, archaea, and protozoa. The intrinsic microbiota differs across different phases of development in insects and is linked to the gastrointestinal tract, cuticle, and other anatomical compartments. According to the scientific papers reviewed, fresh edible insects generally contain significant microbial loads. The main microbial concerns of edible insects include high total counts of mesophilic aerobic bacteria (3.6–9.4 log cfu/g) and the presence of spore-forming bacteria (0.5–5.8 log cfu/g) that can withstand heat treatment; for example, Enterococcaceae (4.2–7.8 log cfu/g), Staphylococcaceae, yeast and molds (3.4–7.2 log cfu/g), lactic acid bacteria (5.2–9.1 log cfu/g), psychrotrophic aerobes (4.5–7.2 log cfu/g), and Enterobacteriaceae (3 log cfu/g threshold) [32]. Insects may also carry food spoilage, harmful microorganisms, and perhaps pathogenic species [33]. However, all the genera are involved in specific effects on the food safety of edible insects, making them indicators of hygiene. The global microbial load of a food sample can be ascertained by counting all mesophilic aerobes; this will also reveal the sample’s overall contamination and microbiological quality. They can also be used to forecast the shelf-life of products held at room temperature. The presence of Enterobacteriaceae in the microbiota of edible insects suggests that they were not degutted or handled under adequate sanitary settings. Usually found in soil and dust, spore-forming bacteria can develop endospores that are difficult to eradicate due to their resistance to heat, dehydration, radiation, and chemicals. Since certain species of lactic acid bacteria (LAB) generate compounds that are good for human health or have probiotic potential, they are typically regarded as healthy, though some species can be poisonous. Psychrotrophic bacteria can cause food spoiling and should be considered while storing edible insects at low temperatures. Interestingly, properly processed edible insects have a trace amount of these microbiota. Boiling, sun-drying, and frying decrease the microbial counts in grasshoppers [19,23]. Enterobacteriaceae in fresh mealworms and small and large crickets can be reduced by boiling, roasting, and stir-frying [16,17,18]. Degutting is another way to avoid microbial contamination.
On the contrary, livestock have complicated microbial compositions with a variety of species numbers. Cattle, pig, sheep, and chicken guts contain a huge diversity of microbiota, the majority portion of which are bacteriocides and firmicutes, followed by actinobacter. The majority of gut microbiome studies in livestock have focused on the characterization of microbial communities using 16S rRNA gene amplicon sequencing as a result of the differences in animal diet composition, gastrointestinal tract (GIT) location, feed efficiency, breed specificity, metabolic disturbances, changes over time, and individual specificities, as well as across housing types and farms. A total of 80–90% of livestock microbiota is composed of bacteriocides and firmicutes. Other taxa include actinobacteria, proteobacteria, spirochaetes, tenericutes, verrucomicrobia, fibrobacteres, etc., differing in abundance between the host species [34,35]. Livestock contains thousands of species, including opportunistic and harmful microbes. As a result, ARGs become more prevalent and resistant to a wide range of antibiotics. For instance, 30 ARGs correlated with colistin and daptomycin were detected in the rumen of sheep [36]. Non-ruminant livestock species face an even more difficult predicament. Major ARGs in hens are similar to those found in pigs, including tetracycline, aminoglycoside, and macrolide–lincosamide–streptogramin [37] (Figure 2).
Vertical transmission is the term for the process by which ARGs can multiply through genetic transfer within the same species of these bacteria. Resistance genes allow a species to adapt and live in circumstances where antibiotics are present. This happens when these genes are passed down from one generation to the next. Since the intestinal ecosystem of edible insects is less diverse than that of animals, there is likely less frequency of this genetic transfer.

3.2. Diet and Antibiotics

Diet is the main culprit for the potential risk factors in the food source. The main diet for edible insects is plant-based substrates like grains or dry vegetables. They eat things we normally do not eat, like apple cores and vegetable waste. Insect diets differ (for example, grasshoppers feed on grass, but Tenebrio molitor grows primarily on grain matrices). While livestock also feed on plant-based diets such as corn, soybeans, sorghum, oats, and barley, there is a plethora of research for improved and composed diets. However, antibiotics are often used as growth promoters to acquire more meat and to encourage livestock’s rapid growth [38]. In the case of insects, there is seldom a need for antibiotics and growth promoters. As regular exposure to antibiotics for the long term is one of the main reasons for ARG abundance, edible insects can easily dodge this bullet.

3.3. Environmental Factors

Horizontal transfer, pollution, and waste production are environmental factors worth mentioning. ARGs are largely dispersed by horizontal gene transfer from the environment. Bacteria can use processes, including transformation, transduction, and conjugation, to pick up resistance genes from their environment, such as soil or water. As a result, bacteria acquire novel resistance features that increase their chances of surviving in settings where antibiotics are abundant. Antibiotics are not the only substances that select ARGs; therefore, this co-occurrence is significant. ARG growth may also be aided by environmental heavy metal pressure, which co-selects antibiotic and metal resistance. Studies reveal that selection for antibiotic resistance is also driven by the co-selection of genes resistant to other toxic substances, including disinfectants, nanomaterials, and biocides [39,40,41]. The amount of ARGs in bacteria containing aromatic degradation genes (ADGs) is more than double that of bacteria without ADGs [42]. P-nitrophenol, p-aminophenol, and phenol are examples of phenolic compounds that have been shown in a study to dramatically raise the frequency of ARG horizontal transfer [43].
Livestock produce a large amount of excrement and are visibly high in ARGs, which can contaminate land, water, and air. Conventional livestock waste treatment does not completely remove antibiotic-resistant bacteria (ARBs), causing their release into soil and water environments [44]. Research shows swine and chicken farms have higher ARG concentrations than hospital and municipal wastewaters, possibly due to higher levels of residual antibiotics from consistent antibiotic use [45]. Edible insects produce little or no waste because they are consumed whole. Moreover, insect farming is a sustainable approach that involves feeding insects with agricultural waste, such as unwanted plant stems and food scraps, in order to promote circular economies. These insects could consume food and biomass that would otherwise go to waste, promoting resource recycling and reuse. They may carry a significant number of bacteria on the surface and within their bodies, which can only be safely consumed if properly treated and kept [10]. Antimicrobial peptides are easily detected in edible insects, specific in types, and have already been linked to significant health benefits [46].
Conclusively, edible insects may offer a more sustainable and safer protein source compared to conventional livestock due to their lower prevalence of ARGs, reduced antibiotic usage in production, and minimal environmental impact. Edible insects benefit from a less diverse gut microbiome, reduced antibiotic exposure, and a more sustainable farming model, suggesting a potentially lower risk of ARG dissemination.

4. Pertinence of Edible Insects over Livestock: Our Perspective

The global food transformation system is undergoing a paradigm shift as we grapple with pressing challenges such as climate change, food insecurity, and the emergence of ARGs. The unsustainable practices of traditional livestock farming, coupled with the growing demand for protein, have created a pressing need for innovative and sustainable food sources. Edible insects, once considered a niche culinary curiosity, are emerging as promising solutions. Their nutritional value, environmental benefits, and potential to mitigate the threat of antibiotic resistance make them a compelling addition to our dietary repertoire.
One of the most pressing concerns in the global food system is the increasing prevalence of ARGs, driven by the overuse of antibiotics in agriculture and medicine. Edible insects, which typically require fewer antibiotics compared to livestock, offer a potential solution to this problem. Do edible insects contain more ARGs than livestock? Our hypothesis is edible insects have a higher possibility of being safer than livestock in the context of ARGs. The basis of this concept is the simple and changeable gut microbiome of edible insects, as well as their extensive AMP production. The abundance of ARGs can occur in three ways: it is transferred genetically among the same species, horizontal transfer from the environment, and long-term exposure to antibiotics. The advantage of edible insects is that their food safety assessment can be maintained due to their easy farming process and their simple structure and gut microbiota composition (Figure 3).
The first thing to be addressed is the safe treatment of rearing feed substrate. Ensuring contamination-free and hygienic feed is critical to healthy insect production. This is to ensure that “disinfecting the feed “and maintaining a “closed environment” for rearing are the best approaches. A closed environment can be maintained using “compartmental architecture” with climate-controlled rearing. As edible insects mature from larvae to adults, their gut microbial diversity varies. Therefore, certain bacteria are shredded, limiting the accumulation of ARGs. Genetic breeding and engineering can aid in this natural phenomenon of acquiring risk-free edible insects to rear industrially. This results in the establishment of a regulatory framework for edible insect cultivation. “Edible insects” must be considered “animal food” instead of “filth”, and risk assessment should be placed in every step from rearing to packaging. Nevertheless, insect farmers can adhere to livestock rules with few alterations. The actual challenge is to see if the regulations can be generalized for all edible insect species. Another important fact is that the processing methods for edible insects can reduce the microbiological risk to close to zero. Evidence showed that properly processed edible insects (dried, boiled, and powdered) had an ignorable presence of ARGs [18,47]. Last but not least, edible insects must be appealingly promoted as food. Every region can raise the insects they have in large quantities, but without consumer appeal, the industry will not establish itself successfully (Figure 4).
In regards to ARGs in edible insects, there is undoubtedly an enormous investigation dearth. Most of the research is still focused on the nutritional value of edible insects. ARGs in livestock have been studied more extensively, but they still lack a regional viewpoint. As we endeavor to comprehend the intricate workings of food production and antibiotic resistance in both food sources, future research holds immense potential to shed light on key aspects of this issue. Future research could focus on the prevalence and transmission dynamics of ARGs in edible insects and livestock, examining the mechanisms driving their dissemination and the impact of different farming practices on antibiotic resistance. To find the safe frequency of ARGs and provide a comparison, ARGs for edible insects and livestock should be calculated based on a sample per unit. For example, examining 1 kg of beef and 1 kg of T. molitor larvae simultaneously, either in their raw or processed forms. An extensive metagenomic study with more parameters and regional comparisons will be a key stepping stone. Identifying sustainable farming methods that minimize antibiotic use while promoting animal health and welfare can lead to a more resilient and environmentally friendly food system. Advancements in molecular biology and genomics offer opportunities for precision monitoring and surveillance of ARGs in both species. Resolving antibiotic resistance in food production systems requires multidisciplinary research and the incorporation of knowledge from ecology, public health, agriculture, and microbiology. Significant improvements and the implementation of evidence-based solutions require the cooperation of researchers, politicians, industry stakeholders, and consumers. As we strive to create a more sustainable and resilient food system, edible insects can unlock the potential to shape a healthier and more sustainable future. As awareness of their nutritional benefits and environmental advantages grows, cultural acceptance is likely to increase. Advancements in food technology and processing techniques will make edible insects more palatable and accessible to a wider audience.

Author Contributions

Conceptualization, X.X.; validation, R.N.R., L.Z. and R.C.; formal analysis, R.N.R.; investigation, R.N.R.; resources, R.N.R. and L.Z.; data curation, R.N.R.; writing—original draft preparation, R.N.R.; writing—review and editing, R.N.R., L.Z., R.C. and X.X.; visualization, R.N.R. and R.C.; supervision, X.X.; project administration, X.X.; funding acquisition, L.Z. All authors have read and agreed to the published version of the manuscript.

Funding

This study was supported by the National Key R&D Program of China (Grant No: 2023YFF1103803) and the Central Public-Interest Scientific Institution Basal Research Fund (Grant No. MFSJKF2024-8).

Data Availability Statement

The original contributions presented in the study are included in the article, further inquiries can be directed to the corresponding author.

Conflicts of Interest

The authors have no conflicts of interest to declare.

References

  1. Pandey, S.; Doo, H.; Keum, G.B.; Kim, E.S.; Kwak, J.; Ryu, S.; Choi, Y.; Kang, J.; Kim, S.; Lee, N.R.; et al. Antibiotic Resistance in Livestock, Environment and Humans: One Health Perspective. J. Anim. Sci. Technol. 2024, 66, 266–278. [Google Scholar] [CrossRef] [PubMed]
  2. Zhen, X.; Stålsby Lundborg, C.; Sun, X.; Zhu, N.; Gu, S.; Dong, H. Economic Burden of Antibiotic Resistance in China: A National Level Estimate for Inpatients. Antimicrob. Resist. Infect. Control 2021, 10, 5. [Google Scholar] [CrossRef]
  3. Zhang, C.; Fu, X.; Liu, Y.; Zhao, H.; Wang, G. Burden of Infectious Diseases and Bacterial Antimicrobial Resistance in China: A Systematic Analysis for the Global Burden of Disease Study 2019. Lancet Reg. Health West. Pac. 2024, 43, 100972. [Google Scholar] [CrossRef] [PubMed]
  4. Tzachor, A.; Richards, C.E.; Holt, L. Future Foods for Risk-Resilient Diets. Nat. Food 2021, 2, 326–329. [Google Scholar] [CrossRef] [PubMed]
  5. Stull, V.J.; Weir, T.L. Chitin and Omega-3 Fatty Acids in Edible Insects Have Underexplored Benefits for the Gut Microbiome and Human Health. Nat. Food 2023, 4, 283–287. [Google Scholar] [CrossRef] [PubMed]
  6. Choi, Y.S.; Lee, J.H.; Kim, T.K.; Shin, D.M. Edible Insects in Food. Adv. Food Nutr. Res. 2024, 108, 223–264. [Google Scholar] [CrossRef]
  7. Rivas-Navia, D.M.; Dueñas-Rivadeneira, A.A.; Dueñas-Rivadeneira, J.P.; Aransiola, S.A.; Maddela, N.R.; Prasad, R. Bioactive Compounds of Insects for Food Use: Potentialities and Risks. J. Agric. Food Res. 2023, 14, 100807. [Google Scholar] [CrossRef]
  8. Milanović, V.; Osimani, A.; Pasquini, M.; Aquilanti, L.; Garofalo, C.; Taccari, M.; Cardinali, F.; Riolo, P.; Clementi, F. Getting Insight into the Prevalence of Antibiotic Resistance Genes in Specimens of Marketed Edible Insects. Int. J. Food Microbiol. 2016, 227, 22–28. [Google Scholar] [CrossRef]
  9. 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. [Google Scholar] [CrossRef]
  10. Li, M.; Mao, C.; Li, X.; Jiang, L.; Zhang, W.; Li, M.; Liu, H.; Fang, Y.; Liu, S.; Yang, G.; et al. Edible Insects: A New Sustainable Nutritional Resource Worth Promoting. Foods 2023, 12, 4073. [Google Scholar] [CrossRef]
  11. Ghimpețeanu, O.M.; Pogurschi, E.N.; Popa, D.C.; Dragomir, N.; Drăgotoiu, T.; Mihai, O.D.; Petcu, C.D. Antibiotic Use in Livestock and Residues in Food—A Public Health Threat: A Review. Foods 2022, 11, 1403. [Google Scholar] [CrossRef] [PubMed]
  12. Brown, J.J.; Jandová, A.; Jeffs, C.T.; Higgie, M.; Nováková, E.; Lewis, O.T.; Hrček, J. Microbiome Structure of a Wild Drosophila Community along Tropical Elevational Gradients and Comparison to Laboratory Lines. Appl. Env. Microbiol. 2023, 89, e0009923. [Google Scholar] [CrossRef] [PubMed]
  13. Woodhams, D.C.; Bletz, M.C.; Becker, C.G.; Bender, H.A.; Buitrago-Rosas, D.; Diebboll, H.; Huynh, R.; Kearns, P.J.; Kueneman, J.; Kurosawa, E.; et al. Publisher Correction: Host-Associated Microbiomes Are Predicted by Immune System Complexity and Climate. Genome Biol. 2020, 21, 40. [Google Scholar] [CrossRef] [PubMed]
  14. Ignasiak, K.; Maxwell, A. Antibiotic-Resistant Bacteria in the Guts of Insects Feeding on Plants: Prospects for Discovering Plant-Derived Antibiotics. BMC Microbiol. 2017, 17, 223. [Google Scholar] [CrossRef] [PubMed]
  15. Osimani, A.; Milanović, V.; Cardinali, F.; Garofalo, C.; Clementi, F.; Ruschioni, S.; Riolo, P.; Isidoro, N.; Loreto, N.; Galarini, R.; et al. Distribution of Transferable Antibiotic Resistance Genes in Laboratory-Reared Edible Mealworms (Tenebrio molitor L.). Front. Microbiol. 2018, 9, 2702. [Google Scholar] [CrossRef] [PubMed]
  16. Roncolini, A.; Cardinali, F.; Aquilanti, L.; Milanović, V.; Garofalo, C.; Sabbatini, R.; Abaker, M.S.S.; Pandolfi, M.; Pasquini, M.; Tavoletti, S.; et al. Investigating Antibiotic Resistance Genes in Marketed Ready-to-Eat Small Crickets (Acheta domesticus). J. Food Sci. 2019, 84, 3222–3232. [Google Scholar] [CrossRef]
  17. Osimani, A.; Cardinali, F.; Aquilanti, L.; Garofalo, C.; Roncolini, A.; Milanović, V.; Pasquini, M.; Tavoletti, S.; Clementi, F. Occurrence of Transferable Antibiotic Resistances in Commercialized Ready-to-Eat Mealworms (Tenebrio molitor L.). Int. J. Food Microbiol. 2017, 263, 38–46. [Google Scholar] [CrossRef]
  18. Grispoldi, L.; Karama, M.; El-Ashram, S.; Saraiva, C.M.; García-Díez, J.; Chalias, A.; Barbera, S.; Cenci-Goga, B.T. Hygienic Characteristics and Detection of Antibiotic Resistance Genes in Crickets (Acheta domesticus) Breed for Flour Production. Microbiol. Res. 2021, 12, 503–512. [Google Scholar] [CrossRef]
  19. Milanović, V.; Osimani, A.; Roncolini, A.; Garofalo, C.; Aquilanti, L.; Pasquini, M.; Tavoletti, S.; Vignaroli, C.; Canonico, L.; Ciani, M.; et al. Investigation of the Dominant Microbiota in Ready-to-Eat Grasshoppers and Mealworms and Quantification of Carbapenem Resistance Genes by QPCR. Front. Microbiol. 2018, 9, 3036. [Google Scholar] [CrossRef]
  20. Vandeweyer, D.; Milanović, V.; Garofalo, C.; Osimani, A.; Clementi, F.; Van Campenhout, L.; Aquilanti, L. Real-Time PCR Detection and Quantification of Selected Transferable Antibiotic Resistance Genes in Fresh Edible Insects from Belgium and the Netherlands. Int. J. Food Microbiol. 2019, 290, 288–295. [Google Scholar] [CrossRef]
  21. Yang, J.; Ju, Z.; Yang, Y.; Zhao, X.; Jiang, Z.; Sun, S. Serotype, Antimicrobial Susceptibility and Genotype Profiles of Salmonella Isolated from Duck Farms and a Slaughterhouse in Shandong Province, China. BMC Microbiol. 2019, 19, 202. [Google Scholar] [CrossRef] [PubMed]
  22. Diana, J. Risk Factors Associated with the Abundance of Antimicrobial Resistance Gene Tet(W) and Class 1 Integron (Intl1) in Pigs in the Netherlands. Utrecht University Student Theses Repository. 2023. Available online: https://studenttheses.uu.nl/handle/20.500.12932/45525 (accessed on 10 September 2024).
  23. Osimani, A.; Garofalo, C.; Aquilanti, L.; Milanović, V.; Cardinali, F.; Taccari, M.; Pasquini, M.; Tavoletti, S.; Clementi, F. Transferable Antibiotic Resistances in Marketed Edible Grasshoppers (Locusta migratoria migratorioides). J. Food Sci. 2017, 82, 1184–1192. [Google Scholar] [CrossRef] [PubMed]
  24. Zou, W.; Jin, C.X.; Wei, S.; Kumar, R.R.; Zhou, Q.X. Occurrence of Antibiotic Resistance Genes in Livestock Farms of Different Scales in North China. J. Agro-Environ. Sci. 2020, 39, 2640–2652. [Google Scholar] [CrossRef]
  25. Xiong, W.; Yang, J.; Zeng, J.; Xiao, D.; Tong, C.; Zeng, Z. Metagenomic Analysis of Antimicrobial Resistance in Ducks, Workers, and the Environment in Duck Farms, Southern China. Ecotoxicol. Env. Saf. 2023, 262, 115191. [Google Scholar] [CrossRef]
  26. Pholwat, S.; Pongpan, T.; Chinli, R.; Rogawski McQuade, E.T.; Thaipisuttikul, I.; Ratanakorn, P.; Liu, J.; Taniuchi, M.; Houpt, E.R.; Foongladda, S. Antimicrobial Resistance in Swine Fecal Specimens across Different Farm Management Systems. Front. Microbiol. 2020, 11, 1238. [Google Scholar] [CrossRef]
  27. Liu, Z.; Wang, K.; Zhang, Y.; Xia, L.; Zhao, L.; Guo, C.; Liu, X.; Qin, L.; Hao, Z. High Prevalence and Diversity Characteristics of Bla NDM, Mcr, and Bla ESBLs Harboring Multidrug-Resistant Escherichia Coli from Chicken, Pig, and Cattle in China. Front. Cell. Infect. Microbiol. 2022, 11, 755545. [Google Scholar] [CrossRef]
  28. Lim, S.K.; Kim, D.; Moon, D.C.; Cho, Y.; Rho, M. Antibiotic Resistomes Discovered in the Gut Microbiomes of Korean Swine and Cattle. Gigascience 2020, 9, giaa043. [Google Scholar] [CrossRef]
  29. Zhang, Y.; Zhang, N.; Wang, M.; Luo, M.; Peng, Y.; Li, Z.; Xu, J.; Ou, M.; Kan, B.; Li, X.; et al. The Prevalence and Distribution of Aminoglycoside Resistance Genes. Biosaf. Health 2023, 5, 14–20. [Google Scholar] [CrossRef]
  30. Dong, W.L.; Kong, L.C.; Wang, Y.; Gou, C.L.; Xu, B.; Ma, H.X.; Gao, Y.H. Aminoglycoside Resistance of Trueperella Pyogenes Isolated from Pigs in China. J. Vet. Med. Sci. 2017, 79, 1836–1839. [Google Scholar] [CrossRef]
  31. Luiken, R.E.C.; Van Gompel, L.; Munk, P.; Sarrazin, S.; Joosten, P.; Dorado-García, A.; Borup Hansen, R.; Knudsen, B.E.; Bossers, A.; Wagenaar, J.A.; et al. Associations between Antimicrobial Use and the Faecal Resistome on Broiler Farms from Nine European Countries. J. Antimicrob. Chemother. 2019, 74, 2596–2604. [Google Scholar] [CrossRef]
  32. Garofalo, C.; Milanović, V.; Cardinali, F.; Aquilanti, L.; Clementi, F.; Osimani, A. Current Knowledge on the Microbiota of Edible Insects Intended for Human Consumption: A State-of-the-Art Review. Food Res. Int. 2019, 125, 108527. [Google Scholar] [CrossRef] [PubMed]
  33. Belluco, S.; Losasso, C.; Maggioletti, M.; Alonzi, C.C.; Paoletti, M.G.; Ricci, A. Edible Insects in a Food Safety and Nutritional Perspective: A Critical Review. Compr. Rev. Food Sci. Food Saf. 2013, 12, 296–313. [Google Scholar] [CrossRef]
  34. Sun, J.; Liao, X.P.; D’Souza, A.W.; Boolchandani, M.; Li, S.H.; Cheng, K.; Luis Martínez, J.; Li, L.; Feng, Y.J.; Fang, L.X.; et al. Environmental Remodeling of Human Gut Microbiota and Antibiotic Resistome in Livestock Farms. Nat. Commun. 2020, 11, 1427. [Google Scholar] [CrossRef] [PubMed]
  35. Forcina, G.; Pérez-Pardal, L.; Carvalheira, J.; Beja-Pereira, A. Gut Microbiome Studies in Livestock: Achievements, Challenges, and Perspectives. Animals 2022, 12, 3375. [Google Scholar] [CrossRef]
  36. Hitch, T.C.A.; Thomas, B.J.; Friedersdorff, J.C.A.; Ougham, H.; Creevey, C.J. Deep Sequence Analysis Reveals the Ovine Rumen as a Reservoir of Antibiotic Resistance Genes. Environ. Pollut. 2018, 235, 571–575. [Google Scholar] [CrossRef]
  37. Ma, T.; McAllister, T.A.; Guan, L.L. A Review of the Resistome within the Digestive Tract of Livestock. J. Anim. Sci. Biotechnol. 2021, 12, 121. [Google Scholar] [CrossRef]
  38. Manyi-Loh, C.; Mamphweli, S.; Meyer, E.; Okoh, A. Antibiotic Use in Agriculture and Its Consequential Resistance in Environmental Sources: Potential Public Health Implications. Molecules 2018, 23, 795. [Google Scholar] [CrossRef]
  39. Wales, A.D.; Davies, R.H. Co-Selection of Resistance to Antibiotics, Biocides and Heavy Metals, and Its Relevance to Foodborne Pathogens. Antibiotics 2015, 4, 567–604. [Google Scholar] [CrossRef]
  40. Ferro, G.; Guarino, F.; Castiglione, S.; Rizzo, L. Antibiotic Resistance Spread Potential in Urban Wastewater Effluents Disinfected by UV/H2O2 Process. Sci. Total Environ. 2016, 560–561, 29–35. [Google Scholar] [CrossRef]
  41. Ma, Y.; Metch, J.W.; Yang, Y.; Pruden, A.; Zhang, T. Shift in Antibiotic Resistance Gene Profiles Associated with Nanosilver during Wastewater Treatment. FEMS Microbiol. Ecol. 2016, 92, fiw022. [Google Scholar] [CrossRef]
  42. Xia, J.; Sun, H.; Zhang, X.; Zhang, T.; Ren, H.; Ye, L. Aromatic Compounds Lead to Increased Abundance of Antibiotic Resistance Genes in Wastewater Treatment Bioreactors. Water Res. 2019, 166, 115073. [Google Scholar] [CrossRef] [PubMed]
  43. Ma, X.; Zhang, X.; Xia, J.; Sun, H.; Zhang, X.; Ye, L. Phenolic Compounds Promote the Horizontal Transfer of Antibiotic Resistance Genes in Activated Sludge. Sci. Total Environ. 2021, 800, 149549. [Google Scholar] [CrossRef] [PubMed]
  44. Li, B.; Yang, Y.; Ma, L.; Ju, F.; Guo, F.; Tiedje, J.M.; Zhang, T. Metagenomic and Network Analysis Reveal Wide Distribution and Co-Occurrence of Environmental Antibiotic Resistance Genes. ISME J. 2015, 9, 2490–2502. [Google Scholar] [CrossRef] [PubMed]
  45. He, Y.; Yuan, Q.; Mathieu, J.; Stadler, L.; Senehi, N.; Sun, R.; Alvarez, P.J.J. Antibiotic Resistance Genes from Livestock Waste: Occurrence, Dissemination, and Treatment. NPJ Clean. Water 2020, 3, 4. [Google Scholar] [CrossRef]
  46. Teixeira, C.S.S.; Villa, C.; Costa, J.; Ferreira, I.M.P.L.V.O.; Mafra, I. Edible Insects as a Novel Source of Bioactive Peptides: A Systematic Review. Foods 2023, 12, 2026. [Google Scholar] [CrossRef]
  47. Chioma, N.; Onoriode, C.E.; Abiye, A.I. Occurrence of Virulent and Antibiotic Resistant Staphylococcus Species in Ready-to-Eat Rhynchophorus Phoenicis and Archachatina Marginata Vended along the Port Harcourt-Bayelsa Route. Afr. J. Microbiol. Res. 2021, 15, 107–119. [Google Scholar] [CrossRef]
Figure 1. Comparison of prevalent ARGs in Dutch, Belgian, Italian, Chinese, Thai, and French edible insects and livestock based on 5 major antibiotic-resistant genes according to the available literature. Color shades change based on the frequency, where the red shade has the highest frequency and the yellow shade has a comparatively low frequency of ARG occurrence. Locations are based on our compared evidential literature.
Figure 1. Comparison of prevalent ARGs in Dutch, Belgian, Italian, Chinese, Thai, and French edible insects and livestock based on 5 major antibiotic-resistant genes according to the available literature. Color shades change based on the frequency, where the red shade has the highest frequency and the yellow shade has a comparatively low frequency of ARG occurrence. Locations are based on our compared evidential literature.
Foods 13 03257 g001
Figure 2. Comparison based on the reason for ARGs’ abundance in edible insects and livestock.
Figure 2. Comparison based on the reason for ARGs’ abundance in edible insects and livestock.
Foods 13 03257 g002
Figure 3. Proposed sequence for food safety regarding edible insects.
Figure 3. Proposed sequence for food safety regarding edible insects.
Foods 13 03257 g003
Figure 4. Sustainable metamorphosis for establishing edible insect convenience.
Figure 4. Sustainable metamorphosis for establishing edible insect convenience.
Foods 13 03257 g004
Table 1. Occurrence of ARGs in edible insects.
Table 1. Occurrence of ARGs in edible insects.
InsectScientific NameCountryBacteriaMethodsARGsAntibioticsRef.
Small cricketsAcheta domesticusNetherlands MarketStreptococcus pyogenes 7008nested PCRtet (O) [8]
Small cricketsAcheta domesticusNetherlands MarketLactobacillus casei/paracasei ILC2279PCRtet (M) [8]
LocustsLocusta migratoriaNetherlands MarketStaphylococcus aureus COL.PCRtet(K) [8]
Mealworm larvaeTenebrio molitorNetherlands MarketStaphylococcus aureus COL.; Enterococcus italicus 1102; Staphylococcus aureus COL.PCRtet(M), tet(S), tet(K) [8]
Giant waterbugsBelostomatidaeThailand MarketEnterococcus hirae Api 2.16; Staphylococcus aureus COL.; Staphylococcus aureus ATCC 2921nested PCRerm(B); tet(K); blaZ [8]
Black antsPolyrhachisThailand MarketStaphylococcus aureus COL.PCRtet(K) [8]
Black antsPolyrhachisThailand MarketStaphylococcus aureus COL.nested PCRerm(B); erm(C); blaZ [8]
Winged termite alatesTermitoidaeThailand MarketEnterococcus hirae Api 2.16; Staphylococcus spp. SE12; Enterococcus italicus 1102; Staphylococcus aureus COL.; Staphylococcus aureus ATCC 2921nested PCRerm(B); erm(C); tet(S), tet(K); blaZ [8]
Rhino beetlesHyboschema contractumThailand MarketEnterococcus hirae Api 2.16; Enterococcus italicus 1102; Staphylococcus aureus COL.; Staphylococcus aureus ATCC 2921nested PCRerm(B); tet(S), tet(K); blaZ [8]
Mole cricketsGryllotalpidaeThailand MarketEnterococcus italicus 1102; Staphylococcus aureus COL.PCRerm(B); tet(S), tet(K) [8]
Mole cricketsGryllotalpidaeThailand MarketStaphylococcus aureus ATCC 2921nested PCRblaZ [8]
Silkworm pupaeBombyx moriThailand MarketEnterococcus italicus 1102; Staphylococcus aureus COL.; Staphylococcus aureus ATCC 2921nested PCRtet(S), tet(K); blaZ [8]
Black scorpionsHeterometrus longimanusThailand MarketEnterococcus italicus 1102; Staphylococcus aureus COL.PCRtet(S), tet(K) [8]
Giant Line Green Stick insectDiaphroedes gigantea Sphingobacterium multivorumbroth microdilution assay Tetracycline[14]
Giant Line Green Stick insectDiaphroedes gigantea Microbacterium oxydans,broth microdilution assay Ciprofloxacin; Tetracycline[14]
Giant Line Green Stick insectDiaphroedes gigantea Bacillus amyloliquefaciensbroth microdilution assay Ciprofloxacin; Tetracycline[14]
Diamondback mothPlutella xylostella Sanguibacter keddieiibroth microdilution assay Ampicillin; Chloramphenicol; Ciprofloxacin; Kanamycin[14]
Diamondback mothPlutella xylostella Raoultella terrigenabroth microdilution assay Ampicillin; Chloramphenicol; Kanamycin; Rifampicin[14]
Cinnabar mothTyria jacobeae Bacillus licheniformisbroth microdilution assay Ampicillin; Chloramphenicol; Tetracycline[14]
Cinnabar mothTyria jacobeae Staphylococcus epidermidisbroth microdilution assay Ampicillin; Kanamycin[14]
Cinnabar mothTyria jacobeae Staphylococcus warneribroth microdilution assay Ciprofloxacin; Rifampicin; Tetracycline[14]
Cinnabar mothTyria jacobeae Burkholderia fungorumbroth microdilution assay Ciprofloxacin; Kanamycin[14]
Death’s-head HawkmothAcherontia atropos Enterobacter asburiaebroth microdilution assay Ampicilin; Chloramphenicol; Ciprofloxacin; Kanamycin; Rifamplcin; Tetracycline[14]
Death’s-head HawkmothAcherontia atropos Pseudomonas putidabroth microdilution assay Chloramphenicol; Kanamycin; Rifampicin; Tetracycline[14]
Death’s-head HawkmothAcherontia atropos Roultella terrigenabroth microdilution assay Ampicillin; Chloramphenicol; Kanamycin[14]
Beet ArmywormSpodoptera exigua Microbacterium paraoxydansbroth microdilution assay Ampicillin; Ciprofloxacin[14]
Beet ArmywormSpodoptera exigua Bacillus aquimarisbroth microdilution assay Rifampicin; Chloramphenicol; Kanamycin
Beet ArmywormSpodoptera exigua Bacillus vietnamensisbroth microdilution assay Ampicillin; Chloramphenicol; Ciprofloxacin; Kanamycin; Rifampicin[14]
Beet ArmywormSpodoptera exigua Rhizobium pusensebroth microdilution assay Ciprofloxacin; Kanamycin; Tetracycline[14]
Rosemary beetleChrysolina americana Staphylococcus epidermidisbroth microdilution assay Ampicillin; Ciprofloxacin; Kanamycin[14]
Mealworm larvaeTenebrio molitor L. Ampicillin-resistant lactic acid bacteriapour plating Ampicillin[15]
Mealworm larvaeTenebrio molitor L. Vancomycin-resistant lactic acid bacteriapour plating Vancomycin[15]
Mealworm larvaeTenebrio molitor L. Ampicillin-resistant enterococcispeard plating Ampicillin[15]
Mealworm larvaeTenebrio molitor L. HLAR enterococcispread plating Gentamicin[15]
Mealworm larvaeTenebrio molitor L. Vancomycin-resistant enterococcispread plating Vancomycin[15]
Mealworm larvaeTenebrio molitor L. Gentamicin-resistant staphylococcispread plating Gentamicin[15]
Mealworm larvaeTenebrio molitor L. Erythromycin-resistant staphylococcispread plating Erythromycin[15]
Mealworm larvaeTenebrio molitor L. Tetracycline-resistant staphylococcispread plating Tetracycline[15]
Mealworm larvaeTenebrio molitor L. Vancomycin-resistant coagulase-positive staphylococcispread plating Vancomycin[15]
Mealworm larvaeTenebrio molitor L. Ampicillin-resistant Enterobacteriaceaepour plating Ampicillin[15]
Mealworm larvaeTenebrio molitor L. Gentamicin-resistant Enterobacteriaceaepour plating Gentamicin[15]
Mealworm larvaeTenebrio molitor L. Gentamicin-resistant Pseudomonadaceaepour plating Gentamicin[15]
Mealworm larvaeTenebrio molitor L. Enterococcus italicusPCRtet(S) [15]
Mealworm larvaeTenebrio molitor L. Enterococcus hirae Api 2.16; Lactobacillus casei/paracasei ILC2279; Staphylococcus aureus COLN-pcrerm(B); tet(M); tet (K) [15]
CricketsAcheta domesticusAustria, Belgium, France, and the NetherlandsLactic acid bacteria; Enterobacteriaceae; Pseudomonadaceae; Listeria monocytogenesPCRerm(B); erm(C); tet(S), tet(K); tet(S), tet(K); blaZ; aac-aph [16]
MealwormsTenebrio molitor L.BelgiumTotal mesophilic aerobes; spore-forming bacteria; lactic acid bacteria; EnterobacteriaceaePCR; N-pcrerm(B); vanA; tet(M); tet(S); tet(K); aac-aph [16]
MealwormsTenebrio molitor L.Netherlands Total mesophilic aerobes; spore-forming bacteria; lactic acid bacteria; EnterobacteriaceaePCR; N-pcrerm(B); erm(C); tet(M); tet(S); tet(K); mecA; aac-aph [16]
MealwormsTenebrio molitor L.Thailand Total mesophilic aerobes; spore-forming bacteria; lactic acid bacteria; EnterobacteriaceaePCR; N-pcrerm(B); erm (C); tet(O); tet(S); tet(K); mecA; aac-aph [17]
MealwormsTenebrio molitor L.FranceTotal mesophilic aerobes; spore-forming bacteria; lactic acid bacteria; EnterobacteriaceaePCR; N-pcrerm(A); erm(B); erm©; vanA; vanB; tet(M); tet(O); tet(S); tet(K); mecA; blaZ; aac-aph [17]
House cricketAcheta domesticusEuropetotal aerobic mesophilic microbiota, lactobacilli, Enterobacteriaceae, total coliforms, staphylococci, and enterococciPCR; N-pcrtetM [18]
MealwormsTenebrio molitor L.Belgium, the Netherlands, ThailandStaphylococcus sp., Bacillus sp., Weissella sp., Eikenella sp., Exiguobacterium sp.PCR; N-pcrbla(OXA−48); bla(NDM−1); tet(M), tet(K), tet(S); erm(B), erm(C); aac-aph [19]
GrasshopperLocusta migratoria migratorioidesThailandStaphylococcus sp., Bacillus sp., Weissella sp., Eikenella sp., Exiguobacterium sp.PCR; N-pcrblaVIM [19]
GrasshopperLocusta migratoria migratorioidesBelgium, the Netherlands, ThailandStaphylococcus sp., Bacillus sp., Weissella sp., Eikenella sp., Exiguobacterium sp.PCR; N-pcrbla(OXA−48); bla(NDM−1); tet(M), tet(K), tet(S); erm(B), erm(C); aac-aph; blaZ [19]
CricketsAcheta domesticusBelgium and the Netherlands PCR; N-pcrtet(O), tet(K), tet (M), tet(S), erm(B) [20]
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Raka, R.N.; Zhang, L.; Chen, R.; Xue, X. Antibiotic Resistance Genes in Global Food Transformation System: Edible Insects vs. Livestock. Foods 2024, 13, 3257. https://doi.org/10.3390/foods13203257

AMA Style

Raka RN, Zhang L, Chen R, Xue X. Antibiotic Resistance Genes in Global Food Transformation System: Edible Insects vs. Livestock. Foods. 2024; 13(20):3257. https://doi.org/10.3390/foods13203257

Chicago/Turabian Style

Raka, Rifat Nowshin, Lin Zhang, Rui Chen, and Xiaofeng Xue. 2024. "Antibiotic Resistance Genes in Global Food Transformation System: Edible Insects vs. Livestock" Foods 13, no. 20: 3257. https://doi.org/10.3390/foods13203257

APA Style

Raka, R. N., Zhang, L., Chen, R., & Xue, X. (2024). Antibiotic Resistance Genes in Global Food Transformation System: Edible Insects vs. Livestock. Foods, 13(20), 3257. https://doi.org/10.3390/foods13203257

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop