Distribution Characteristics of Antibiotic Resistance Genes in Chinese Livestock, Poultry, and Aquaculture Farms ()
1. Introduction
Antibiotic resistance and microbial evolution have become important causes of increased morbidity and mortality in humans and animals worldwide [1]-[3]. The annual rate of deaths directly caused by AMR is predicted to increase to 10 million by 2050, with the highest estimated deaths being in Asia [4]. Around 100,000 - 200,000 tons of antibiotics are used globally each year [5] and global consumption of veterinary antibiotics is projected to grow by 11.5% in 2030. In China, the use of veterinary antibiotics as feed additives for growth promotion has reached approximately 6000 - 8000 tons per year [6]-[8]. A survey found that the demand for antibiotics in food animals in developing countries continues to increase every year [9]. In different various habitat environments and regions, the effects of different environmental and social activities have led to differences in antibiotic residues. For example, the highest concentration of gentamycin was detected in pig manure in Shandong Province at 754.4 mg/kg, and quinolones, such as norfloxacin and enrofloxacin, were detected in eight provinces of China at 225.45 and 1420.76 mg/kg, respectively [7] [10]. Concentrations of oxytetracycline and sulphadimethoxine were detected in wastewater from nearby pig farms and rivers in Jiangsu at 72.9 and 211 μg/L, respectively [11]. The maximum concentrations of enrofloxacin and ciprofloxacin detected in chicken feces were 61.3 and 18.8 mg/kg, respectively [12]. The levels of antibiotics detected in aquaculture waters generally range from ng∙L−1 levels to µg∙L−1 levels [13].
Antibiotic resistance genes (ARGs) have emerged as a new type of environmental pollutant that poses a major threat to global public health [14] [15]. Various ARGs have been detected in farms, live poultry slaughterhouses, rivers, lakes, sewage treatment plants, municipal water supply systems, medical wastewater, and soil [16]-[22]. Considerable evidence suggested that ARGs and antibiotics are released from livestock and poultry farms into their surroundings that include water, soil and air [23]. Feces and wastewater containing ARBs can reach a wider environment through runoff and atomization [24]-[26] and then spread to humans through the food chain. ARBs and ARGs in the human body are like a “time bomb” with great destructive potential to consistently threaten residents and farm workers’ health [27]. Therefore, exploring the distribution law and characteristics of ARGs in the farm environment and providing suggestions on the use of antibiotics in farms and the prevention of transmission are necessary.
The “One Health” strategy is a cross-sectoral collaborative approach to address the issue of AMR, it focuses on the health of humans, animals, and the environment from the perspective of “One Health” [28]. Therefore, the species and diversity of ARGs in the feces and surrounding environment of different species (swine, cattle, chicken, duck, and aquatic animals) were summarized in the present study. The characteristics of animal breeding and ARG pollution in different regions were compared systematically. The findings could contribute to the full understanding of ARGs in livestock, poultry, and aquaculture farms and their surrounding environment. This research aimed to provide a scientific foundation for controlling the transmission of ARGs and enhancing health management in farms.
2. Methods
2.1. Study Inclusion and Selection
The literature data for this study were searched from the core databases of Web of Science, Pubmed and Embase on August 26, 2023. By Using [(ARGs) OR (antibiotic resistance genes) OR (antimicrobial resistance genes) AND ((animal farms) OR (animal farms) OR (livestock)] AND (China) as the search keywords, ARG information was collected from the full texts of previously published studies searched on the three websites by artificial extraction. The inclusion criteria were as follows: 1) studies reporting the characteristics of ARGs on farms; 2) specific sampling sites, drug resistance gene detection and quantitative methods and 3) articles focusing on the analysis of major ARGs and specific ARG subtypes, with ARGs subtypes available in the attached table. The exclusion criteria were as follows: 1) lack of sampling sites and drug resistance gene testing methods; 2) repeated analysis on the same ARGs in a unified study, and 3) lack of ARG subtypes in reported farms.
2.2. Statistical Analysis and Visualization
The overall distribution of ARGs in Chinese farms was assessed on the basis of the number of reports for each ARG in a collection of 103 articles. The main ARGs present in different farms were calculated by dividing the number of literature reports on a certain gene by the number of literature reports on that farm. The proportion of the top 53 kinds of ARGs in each farm was calculated in accordance with the number of literature reports.
The ARGs data were processed using Microsoft Excel 2016. The website https://www.liuchengtu.com/home/myfile/ was used to make an article screening flow chart. A Sankey diagram was produced on the Pythonol website (https://www.genescloud.cn/chart/ChartOverview). A histogram was created on GraphPad Prism (version 8.0.2). Network analysis was conducted in Gephi platform (version 0.9). Venn diagrams were generated using EVenn [29]. The antibiotic species reported by different farms were visualized using python (version 3.11). The distribution of ARGs in different regions of China was presented using R (version 4.3.1) software.
3. Overall ARG Distribution in Farms
The literature search yielded 1955 nonduplicate publications, of which 103 eligible studies were reviewed in full text (Figure 1). A total of 1627 ARG subtypes extracted from the 103 studies were categorized into 16 ARG types and MGEs. Among them, 79 (77%) studies reported 84 tetracycline resistance gene subtypes, 67 (65%) studies reported 46 sulfonamide resistance gene subtypes, and 53 studies (51%) reported 126 macrolide-lincomycin-streptomycin B (MLSB) resistance gene subtypes, 40 (39%) studies reported 711 beta-lactamase resistance gene subtypes, 38 (37%) studies reported 211 aminoglycoside resistance gene subtypes, 36 (35%) studies reported 47 quinolone resistance gene subtypes, 34 (33%) studies reported 29 mobile genetic elements (MGEs), and 31 (30%) studies reported 146 multidrug resistance gene subtypes (Figure 2).
In accordance with the reported frequency of farm ARGs, the top 53 ARGs (detected in more than three articles) with the largest number of articles were selected, and their proportions in different farms were analyzed (Figure 3). They covered 10
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Figure 1. Articles and screening flow charts collected from Pubmed, Web of science, and Embase.
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Figure 2. The number of ARGs species and literature reports collected in the 103 articles included in this study.
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Figure 3. Reported frequencies of the top 53 ARG subtypes and their respective antibiotic families extracted from Pubmed, Web of science, Embase publications.
antibiotic families: tetracyclines (tet), sulfonamides (sul, and dfr), quinolones (qnr, and oqx), MLSBs (erm, optr, ere, lnu, and mph), aminoglycosides (aad, str, and aph), beta-lactamase (bla), chloramphenicols (cml, and fex), polymyxins (mcr), multi-resistant type (flo), unclassified (cfr) antibiotic types, and MGEs (intI). The sulfonamide ARG subtypes sul1 and sul2 were the highest rates reported in literature, followed by tetracyclines and MLSB.
4. Characteristics of the Regional Distribution of ARGs
China was divided into seven regions: South China, North China, Central China, East China, Southwest, Northwest, and Northeast. The ARG distribution in Southwest, Northwest and Northeast regions into other categories. Most publications were reported in South China, followed by East China, other categories, North China, and Central China. Among the 103 studies of ARGs/MGEs related in farms, 29% (30/103) of studies reported on farms in South China, with 472 ARG subtypes. They were categorized into 14 ARG types and MGEs, of which Guangdong Province reported the highest number of ARGs. In addition, the highest number of ARGs in East China, with 1382 subtypes, belonging to 15 ARG types and MGEs. Among them, the species of ARGs reported in farms in Shandong Province were the most abundant, followed by Fujian Province. The serious ARG pollution in farms in Central China was mainly concentrated in Henan Province (Table 1).
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Table 1. Distribution characteristics of ARGs species in different regions.
In South China, East China, and Central China, sulfonamide ARGs, such as sul1 and sul2, were the type with a high rate of literature report. Moreover, the number of literature reports on tetM in East China was the largest, followed by tetO and tetW. In South China, tetX had the largest number of literature reports, followed by tetM and tetA. In North China, tetW, tetM, and tetO had the largest number of articles, followed by intI1, tetQ, blaTEM-1, intI2, sul1, sul2, and tetC. Similar trends were reported in publications from other regions, indicating widespread antibiotic use in farms throughout China. The distribution of the top 40 ARGs in different regions of China is shown in Figure 4, covering 9 antibiotic families: tetracyclines, sulfonamides, quinolones, aminoglycosides, beta-lactamases, MLSB, multidrugs, other resistant drugs, chloramphenicol, and MGEs. MLSBs (ermB and ermF) were found to be common in Chinese farms. Meanwhile, the sulfonamide ARG dfrA1 was also abundant in South China. The quinolone gene qnrS had the greatest number of literature reports in East China.
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Figure 4. Reported frequency of the top 40 ARG subtypes extracted from Pubmed, Web of science, Embase publications grouped by region.
5. Distributional Characteristics of ARGs in Different Farms
5.1. Livestock Farms
5.1.1. Swine Farms
Among the 103 studies of ARGs related to farms, 54 (52%) articles on pig farms were screened, reporting 1427 ARG subtypes belonging to 16 ARG types and MGEs. The beta-lactamase subtype of ARGs had the highest number of reports, followed by aminoglycosides, multidrug resistance, and MLSB (Table 2; Figure 6(a); Figure 7). Among the first 53 types of ARGs, the reporting rate of beta-lactamase ARGs (blaTEM-1, blaSHV, blaOXA-1, blaCTX?M and blaampC) was the highest. The aminoglycoside ARGs [aph(6)?Id] [and aadA] and some MLSB ARG subtypes were more abundant than in other farms (Figure 5). In addition, among the 54 studies on pig farms, the ARG subtypes with the highest number of literature reports were sulfonamide ARGs (sul1 and sul2), followed by tetracycline ARGs (tetM, tetW, and tetO) and MLSB ARGs (ermB).
Livestock feces is an important reservoir and vehicle for the trans-environmental spread of ARGs [30]. In total, 1272 subtypes of ARGs and MGEs were reported in pig feces, and they were classified into 16 ARG types. Beta-lactamase was the most abundant ARG type, with a total of 533 subtypes, followed by aminoglycosides, multidrugs, and MLSB. A total of 433 subtypes of ARGs and MGEs were reported in wastewater, and they were classified into 15 ARG types. Among various mediators, the wastewater of pig farms, had the largest number of MGEs subtypes. In the soil of pig farms, 512 subtypes of ARGs/MGEs were reported. The amount of beta-lactamase ARGs in soil was higher than in wastewater and air. The aminoglycoside and tetracycline ARGs were more abundant in the air of pig farms (Figure 6(b)).
5.1.2. Cattle Farms
Among the 103 studies of ARGs related to farms, 18% (19/103) of articles on cattle farms were screened, reporting 186 ARG subtypes belonging to 11 ARG types and MGEs. The number of tetracycline ARGs was the highest, followed by beta-lactamase ARGs (Table 2; Figure 6(a)). Among the 19 studies related to cattle farms, the literature reports on sulfonamide ARGs (sul1 and sul2) were the most numerous, followed by tetracycline ARGs (tetW and tetQ). Among the types of farms, cattle farms had the higher number of species with MGE subtypes. Among the first 53 types of ARGs, the literature on quinolone ARG oqxB had the highest proportion, followed by tetT and ermC. Moreover, the reporting rate of aminoglycoside ARG (strB) was higher than that in pig farms (Figure 5).
In feces from cattle farms, 170 ARG subtypes belonging to 11 ARG types and MGEs were reported. Tetracycline and beta-lactamase ARGs had multiple subtypes. The wastewater of cattle farm contained a high number of MLSB ARG subtypes. Similar to the distribution of ARGs in wastewater, the ARGs in cattle farm soil were classified into eight ARG types. Besides intI1 and intI2, intI3, tnpA-01, trb-C, tnpA-02 and tnpA-05 were found in cattle farm soil. Some research data
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Figure 5. Distribution of the top 53 ARG subtypes in different farms.
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Table 2. Article report on antibiotic resistance genes in different farms.
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Figure 6. (a) Types of antibiotics in pig farms, cattle farms, chicken farms, duck farms, aquaculture farms. (b)-(e) Distribution of antibiotic species in feces, wastewater, soil and air from pig, cattle, chicken and duck farms, respectively. (f) Distribution of antibiotic species in aquaculture farms sediments, aquaculture water and animal intestines.
showed that the detection rate of intI1 in all soil samples of dairy farms was 100% [31]. In the air of cattle farms, a total of 101 ARG subtypes were reported, with tetracycline and aminoglycoside ARG subtypes being the most abundant, followed by beta-lactamase and MLSB subtypes (Figure 6(c)).
5.2. Poultry Farms
5.2.1. Chicken Farms
Among the 103 studies of ARGs related to farms, 26% (27/103) of articles reported farm-associated ARGs in chicken farms, including 134 ARG subtypes belonging to 11 ARG types and MGEs (Table 2; Figure 6(a)). Except in pig farms, polymyxin had the largest number of subtypes reported in chicken farms. Among the first 53 subtypes of ARGs, the aminoglycoside ARG (strA) in chicken farms had the highest reporting rate among all farms (Figure 5). Of the 27 studies conducted in chicken farms, sulfonamide ARG subtypes (sul1 and sul2) were reported in 17 and 16 articles, respectively, followed by MLSB ARG (ermB) and tetracycline ARGs tetM and tetG.
Previous studies have shown that the concentration of ARGs in poultry feces was higher than that in livestock [32]-[34]. In the feces of chicken farms, a total of 102 ARG subtypes, belonging to 11 ARG types and MGEs were reported, with beta-lactamase being the most abundant ARG type. In wastewater, with tetracycline was the most abundant ARG type. Twenty-two ARGs were reported in soils, and they were classified into five ARG types. Research has shown that the prevalence of ARGs in agricultural soils may be a source of groundwater pollution through vertical migration [35]. In the air of chicken farms, aminoglycosides had the largest number of subtypes. The high abundance of ARGs in chicken farms may be related to the prevalence of MGEs (Figure 6(d)).
5.2.2. Duckery
Among the 103 studies of ARGs related to farms, 8% (8/103) of articles reported farm-associated ARGs in duck farms, including 347 ARG subtypes, belonging to 12 ARG types and MGEs (Table 2; Figure 6(a); Figure 7). Among them, beta-lactamase had the largest number of subtypes, with 62 species, followed by aminoglycosides, multidrugs and MLSB. Among the first 53 subtypes of ARGs, tet36 had the highest reporting rate, followed by tetL and tetC (Figure 5). In addition, among the eight studies on duck farms, sulfonamide ARGs (sul1 and sul2) still had the largest number of reports, followed by tetA, tetM, and tetC.
In duck feces, a total of 339 ARG subtypes, belonging to 12 ARG types and MGEs were reported (Figure 6(e)). Among them, aminoglycosides, beta-lactamase, MLSB, multidrug, vancomycin, tetracycline had many ARG subtypes. All 34 tetracycline and 17 sulfonamide ARG subtypes in duck farms were present in feces. Thirty subtypes of ARGs were reported in duck farm wastewater, belonging to eight ARG types and MGEs, with tetracycline subtypes being the most abundant.
5.3. Distribution of ARGs in Aquaculture
Aquaculture is one of the fastest growing industries in the world [36]. However,
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Figure 7. Sangki map of antibiotic species in different farms and environmental media.
high-density and mixed farming has led to a decline in water quality and outbreaks of aquatic animal diseases [37], and the consequent high use of antibiotics in feeds and aquaculture medicines has resulted in elevated drug resistance.
Among the 103 studies of ARGs related to farms, 23% (24/103) of articles reported farm-associated ARGs in aquaculture farms, including 165 ARG subtypes, belonging to 12 ARG types and MGEs (Table 2; Figure 6(a)). Among them, β-lactamase subtypes and quantities were the largest, followed by tetracycline and vancomycin. In the first 53 subtypes of ARGs/MGEs, tetracycline ARG subtypes, such as tetB, were the most dominant, followed by tetX (Figure 5). Sul3 had a high reporting rate in aquaculture farms. In addition, among the 24 studies on aquaculture, sul1 and sul2 had the largest number of literature reports, followed by tetracycline ARGs (tetX, and tetB) and multidrug ARG floR.
ARGs are widely distributed in the intestines of aquaculture animals [38]. In total, 70 subtypes of ARGs/MGEs were reported in aquaculture water, and they were classified into 10 ARG types (Figure 6(f)). Tetracycline ARG subtypes were the most abundant, followed by beta-lactamase. A total of 34 ARG subtypes were reported in sediments, including 13 kinds of tetracycline ARGs, which were similar to those in aquaculture water. However, qacED1, bacA, acrB and ompF were mainly present in sediments. The sulfonamide ARGs in sediments mainly included sul1, sul2 and sul3. In addition, the ARGs present in the intestines of cultured fish and shrimp did not considerably differ from the ARGs in cultured sediments. A total of 28 ARG subtypes in animal intestines were reported. Among them, the most diverse ARG types were tetracycline, sulfonamide, and quinolones.
6. Shared and Unique ARGs
ARGs are also likely to be shared among various environmental media in livestock, poultry, and aquaculture farms. Among these shared ARGs, the number of common genes reported in pig, cattle, chicken, duck, and aquaculture farms was 28, belonging to nine ARG types and MGEs. They included tetracycline ARGs (tetA, tetC, tetG, tetM, tetO, tetQ, tetW, tetX, and tetT), sulfonamide ARGs (sul1, sul2, and sul3), MLSB ARGs (ermB, ermC, and ermF), beta-lactamase ARGs (blaOXA-1, and blaTEM), multidrug ARGs (acrA, acrB, and floR), aminoglycoside ARGs (aadA, aadA1, and aadE), quinolone ARGs (qnrA, qnrS, and oqxB), chloramphenicol ARGs (fexA), and other classes of ARGs (cfr). Seven ARG subtypes belonging to four types were shared by aquaculture, pig, cattle, and chicken farms, including quinolone ARGs (qnrB, and qnrD), beta-lactamase ARGs (blaTEM-1, blaGES), vancomycin ARGs (vanA, and vanB) and MGE (intI1). In livestock and poultry farms, 15 ARG subtypes belonging to six types were shared by pig, cattle, and chicken farms, including tetracyclines ARGs (tetS, tetT, and tetB/P), quinolone ARG (qepA), aminoglycoside ARGs [aadA] [aac(6)-lb(akaaacA4)] [and strB], beta-lactamase ARGs (blaOXA-1, blaTEM-1, and blaampC, blaGES-1), multidrug ARGs (acrA, and acrB), other unclassified ARG (catB3), and MGE (intI1). ErmX, ermA, ermQ, tetB/P, tetL, tet32, blaampC, blaNDM, catB3, mefA, and aph(6)Id also shared in swine, cattle, chicken, and duck farms (Figure 8(a), Figure 8(b)).
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Figure 8. (a)-(b) Co-occurrence and number of ARG subtypes in pig farms, cattle farms, chicken farms, duck farms and aquaculture farms. (c) The frequency of literature reports on different farms is greater than or equal to 5.
For the majorly shared ARGs with more than or equal to five articles reports in different farms (Figure 8(c)). The largest number of shared genes was in pig, cattle, chicken, and aquaculture farms, including genes (ermB, tetQ, tetG, ermF, intI1, and qnrS), followed by sul2, tetM, tetW, tetO, and tetX. The results also showed a large number of shared ARGs between pig farms and other farms. The number of ARG subtypes shared by pig and duck farms was the largest, with 217 ARG subtypes, followed by pig and aquaculture farms, with 69 ARG subtypes shared on them. A total of 993 unique ARG subtypes were found in pig farms (Figure 8(a), Figure 8(b)), indicating that the research on ARGs in China was mostly biased towards pig farms.
In this study, a large number of ARG subtypes were shared in the environmental media of different farms (Figure 9). In livestock farms, the most abundant
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Figure 9. Venn diagram of ARGs and quantity shared by different farms and different environmental media. (a) Venn network diagram of ARG subtypes shared in livestock farms and aquafarms. (b) Venn diagram of the number of ARG subtypes shared in livestock farms and aquafarms. (c) Venn network diagram of shared ARG subtypes in livestock farms. (d) Venn diagram of the number of ARG subtypes shared in livestock farms. (e) Venn network diagram of ARG subtypes shared in aquafarms. (f) Venn diagram of the number of ARG subtypes shared in aquafarms.
ARG subtypes were shared in feces, wastewater, and soil, with 283 ARG subtypes, followed by 101 ARG subtypes, shared between feces and soil. From all media in livestock and aquaculture farms, the largest number of genes was shared in feces and soil, with 99 ARG subtypes. In addition, 848 ARG subtypes were specifically present in feces. A total of 52 ARG subtypes were shared among feces, wastewater, soil, and air. Of these 52 ARG subtypes, 15 were shared with sediments, aquatic water, and animal intestines.
7. Discussion
In this systematic review, the distribution characteristics of ARGs in different farms in China from 103 studies were analyzed. The findings indicated that the number and types of ARG reports were the highest in East China, with Shandong Province and Fujian Province being the most polluted. The pig farms in China had the largest number of ARG subtypes and species, followed by duck farms, cattle farms, aquaculture farms, and chicken farms. Antibiotics, ARBs, and ARGs have been reported to be widely distributed in various environmental substrates [39]. Here, the distribution law of ARGs in the feces, soil, wastewater, and air of animal husbandry and poultry farms, and in the aquatic water, sediments, and animal intestines from aquaculture were summarized.
Among the 103 studies on the Chinese farm industry, different degrees of ARG and MGE contamination of tetracycline, sulfonamide, quinolone, aminoglycoside, beta-lactamase, MLSB, multidrug, and chloramphenicol were found in farms from different regions of China. Previous studies have shown that sulfonamides, tetracyclines, quinolones, and macrolides are widely used in modern livestock farm industries [33] [40]. The findings of the present study are consistent with those of previous studies [41]. Furthermore, more research on aquaculture due to the coastal characteristics of South China, so it can be increased in the use of antibiotics in aquaculture in South China of management, especially in Guangdong Province and Guangxi Province. The results also suggested that among the types of ARGs, the number of beta-lactamase ARG subtypes was the highest in pig, duck and aquaculture farms. To date, beta-lactamase antibiotics have been widely applied in livestock husbandry to treat bacterial infections, and resistance to beta-lactamase antibiotics is categorized as high-risk multidrug resistance, which is closely associated with the human health [42]. The results of a study on the distribution of ARGs in the gut of Chinese crayfish, demonstrated that the beta-lactamase class had the highest absolute abundance of the nine resistance genes tested [43], may be due to the high sales of beta-lactamases in aquaculture [44].
Enrichment was most pronounced in animal feces, followed by soil and wastewater. In aquaculture farms, the types and quantities of ARGs in the aquatic water, sediment, and animal intestines were relatively similar (Figure 5). Previous studies have shown that feces samples had the highest abundance and diversity of ARGs, and that they were one of the potential contributors to the surrounding environment and workers [45]. However, studies have shown that, many swine bacterial species cannot survive in the human gut. Moreover, farm workers are more mobile and have a [46] more diverse diet, hence more opportunities to acquire resistance to bacteria [47]. Therefore, the spread of ARGs in farm workers may be influenced by more than the farm environment. ARGs are also abundant in soils around livestock farms and fertilized farmland, the abundance of ARGs in fertilized soil was 2.1 - 138.0 times that in unfertilized soil [48]. The concentrations of ARGs in soil were lower than those in feces, possibly due to the dilution effect of the soil matrix during fertilization. The application of wastewater in farmland is a major route of dissemination of ARGs to the environment, increasing the ARG level in soils and in runoffs [49] [50]. The presence of multiple antibiotics in wastewater fertilization soils has been observed in several studies [51] [52]. Therefore, wastewater, as one of the wastes of animal production, is considered to be a hot environment for antibiotic resistance [53]. Some studies have shown that the relative abundance of ARGs in aquaculture environmental sediments was higher than that in aquaculture water [54]. However, the results of the present study indicated a greater variety and quantity of ARGs in aquaculture water. The reason may be related to different farming practices and environments. Other studies have shown that integrated culture ponds (duck and fish ponds) exhibited the lowest absolute abundance of ARGs in culture waters, and the highest absolute abundance of ARGs was found in sediments [55]. The possible reason is that ARGs spread over time, leading to their long-term accumulation in sediments and enhancing antibiotic resistance [15]. In summary, the difference in the distribution of ARGs in different types of farms may be attributed to the sample types, animal types, and sampling time affecting the detection rate and distribution rule of genes [56].
ARGs may be transferred between bacteria via genetic factors, for instance, MGEs, plasmids, transposons, and integrons, act as resistance genes transmitting agents in different environmental media [57]. The present study found that proportion of MGEs was the highest in the wastewater of cattle and pig farms. In chicken farms, the MGE subtypes mainly existed in soil. A comprehensive study examining ARGs in livestock farms in East China, found 10 tet resistance genes and two sul genes, as well as a genetic element, intl1, associated with mobile ARGs [13] [32]. In broiler farms, tnpA and intl1 were significantly and positively correlated with seven and five ARG subtypes, respectively [58]. The presence of abundant MGE subtypes, including intI1, tnpA, tnpA04, and tnpA-05, in aquatic water, sediments, and animal intestine, may be the reason for the water environment’s ARG contamination levels being similar.
To sum up, the spread of ARGs on farms is a more serious problem in China. Corresponding measures must be taken to rectify the phenomenon of excessive use of veterinary drugs and exceeding residue limits in breeding. First, drug sensitivity tests must be carried out, and correct and efficient antibiotics for large-scale farms to choose from and refer to must be selected. Second, the technical guidance on the use of veterinary antibiotics must be strengthened, and their awareness and level of standardized drug use must be improved. When using antibiotics, the principle of correct usage must be strictly followed, excessive or insufficient use should be avoided, and the combined use of antibiotics should generally not exceed three types. In addition, strengthening the disinfection of the breeding environment and strictly implementing the disinfection and quarantine system are necessary. With the advancement of isotope labeling and fluorescent labeling technologies, the visualization of the ARG propagation process by labeling bacteria, plasmids or other genetic elements to design bonding conditions [59] is an effective means to control ARG propagation and diffusion on the basis of process resistance, and it is the focus of future research.
The limitations of this study must be acknowledged. First, the extraction of ARG diversity and the distribution information of different types of farms had limitations and information biases. One study that contained ARG information on multiple types of farms and media was included in the present study. In the subsequent studies, some scientifically rigorous methods should be used to extract information, and more than two people should be involved in the verification and entry of data.
8. Conclusion
This study showed that the pollution of various types of ARGs is serious in Chinese farms. Nine ARG types were shared in pig, cattle, chicken, duck, and aquaculture farms. ARGs were mainly present in animal feces, followed by soil and wastewater. In aquaculture farms, aquacultural water was the main source and repository of ARGs. Various ARG subtypes in livestock and aquaculture farms have demonstrated certain differences, which may be caused by animal types, breeding conditions, and sample types. The reporting rate of ARGs in farms in South China was the highest, and the number of ARG species in East China was the highest. Overall, the findings provide a scientific basis for corresponding measures to reduce the production and transmission of ARGs in livestock farms.
Acknowledgements
This work was financially supported by the National Science and Technology Specific Projects (grant number2018ZX10301407).
Data Availability
Data generated analyzed during this study are provided in full within the published article.