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. 2023 Feb 6;871:162035. doi: 10.1016/j.scitotenv.2023.162035

Enhance antibiotic resistance and human health risks in aerosols during the COVID-19 pandemic

Qing Wang a, Changzhen Liu a, Shaojing Sun a, Guang Yang a, Jinghui Luo a, Na Wang b, Bin Chen c, Litao Wang a,⁎
PMCID: PMC9901221  PMID: 36754321

Abstract

Aerosols are an important route for the transmission of antibiotic resistance genes (ARGs). Since the 2019 (COVID-19) pandemic, the large-scale use of disinfectants has effectively prevented the spread of environmental microorganisms, but studies regarding the antibiotic resistance of airborne bacteria remain limited. This study focused on four functional urban areas (commercial areas, educational areas, residential areas and wastewater treatment plant) to study the variations in ARG abundances, bacterial community structures and risks to human health during the COVID-19 pandemic in aerosol. The results indicated the abundance of ARGs during the COVID-19 period were up to approximately 13-fold greater than before the COVID-19 period. Large-scale disinfection resulted in a decrease in total bacterial abundance. However, chlorine-resistant bacteria tended to be survived. Among the four functional areas, the diversity and abundance of aerosol bacteria were highest in commercial aera. Antibiotic susceptibility assays suggested elevated resistance of isolated bacteria to several tested antibiotics due to disinfection exposure. The potential exposure risks of ARGs to human health were 2 times higher than before the COVID-19 pandemic, and respiratory intake was the main exposure route. The results highlighted the elevated antibiotic resistance of bacteria in aerosols that were exposed to disinfectants after the COVID-19 pandemic. This study provides theoretical guidance for the rational use of disinfectants and control of antimicrobial resistance.

Keywords: Antimicrobial resistance, Aerosol, Disinfectant, COVID-19, Human health risk

Graphical abstract

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1. Introduction

Antibiotics are widely used to improve human health, animal growth, and feed efficiency (Aguilar-Santelises et al., 2020). However, large quantities of antibiotics have been used and misused, leading to a global antibiotic resistance crisis (Li et al., 2018). At present, ARGs have been detected in a variety of environmental media, such as water (Wu et al., 2020), soil (Xu et al., 2021), air (Li et al., 2020), plants (Chen et al., 2019), and food (Zhang et al., 2019b). Airborne transmission is one of the dissemination pathways of ARGs (Jin et al., 2022; Wang et al., 2022). Bioaerosols are very small airborne particles with diameters of 0.001 to 100 μm, and pathogenic and/or nonpathogenic microorganisms such as viruses, bacteria, and fungi may be present in bioaerosols. The presence of ARGs indicates the potential for transfer of resistance among airborne bacteria (Xie et al., 2019). Antibiotic-resistant bacteria (ARB) in the air, especially pathogenic-resistant bacteria, may cause long-term respiratory diseases and cause potential health crises due to their antibiotic resistance (Mao et al., 2015).

Since the end of 2019, pneumonia caused by SARS-CoV-2 has spread around the world (Bedi et al., 2020). As a precaution, disinfection measures have become more important in homes and high-risk public places (such as educational institutions, health and other care facilities, food service facilities and workplaces). Long-term exposure to biocidal agents can select for antibiotic-resistant strains and increase the risk of cross resistance to antibiotics (Getahun et al., 2020; Kampf, 2018). Ethanol (Pidot et al., 2018) and chlorine-based disinfectants (Tandukar et al., 2013) can facilitate bacterial acquisition of antimicrobial resistance through mutation or horizontal gene transfer. Improper use of biocides (e.g., cationic agents and triclosan) when spraying, fogging streets or in marketplaces (Subramanya et al., 2021) could select resistant bacteria (Capita et al., 2019). Furthermore, bacteria are more likely to develop resistance due to the increased use of disinfectants since the COVID-19 pandemic (Lu and Guo, 2021). However, conflicting results have been reported that chlorination in water treatment was effective in reducing ARGs and mobile genetic elements (MGEs) rather than co-selecting them (Lin et al., 2016). Therefore, we presumed that extensive use of disinfectants may change bacterial resistance in aerosols and further pose potential risks to human health.

To obtain insights into these issues, we investigated the distributions of 5 common ARG types, including 11 ARG subtypes and bacterial community structures, in four functional areas (e.g., commercial areas, educational areas, residential areas and wastewater treatment plant (WWTP)) in Shijiazhuang, Hebei Province. Based on determinations of minimum inhibitory concentrations (MICs) and disinfectant exposure tests conducted in the laboratory, the antibiotic resistance levels of culturable pathogenic strains in aerosols were evaluated. Furthermore, the exposure doses of ARGs through two major pathways, namely, skin exposure and respiratory inhalation, were estimated. This study will aid in assessing antibiotic resistance and human health risks when prophylactic measures such as disinfection during COVID-19 are used.

2. Materials and methods

2.1. Aerosol sample collection

Aerosol samples were collected before and during the COVID-19 pandemic in September 2019 and 2020 in four different functional areas of Shijiazhuang, Hebei, China (Table S1 and S2). The four functional areas included commercial areas (38°1′46.3″N, 114°33′7.4″E), educational areas (38°1′32.9″N, 114°33′21.9″E), residential areas (38°2′10.8″N, 114°33′0.3″E) and WWTP (37°59′48.9″N, 114°28′53.6″E). A liquid aerosol biosampler (228–9620, SKC, USA) with 20 mL of sterile phosphate-buffered saline (PBS) was used to collect aerosol samples at a flow rate of 12.5 L/min and sampling time of 20 min. Three samples were collected at each sampling point and then mixed into one sample. All tools used in the sampling process were sterilized with 75 % alcohol. After sampling, all samples were stored at −20 °C for subsequent analysis.

2.2. Isolation and identification of cultivable airborne bacteria

After sampling, 5 mL samples were used to isolate and identify cultivable airborne bacteria. According to the manufacturer's instructions, Luria-Bertani (LB) solid/liquid media were prepared and autoclaved for 20 min at 121 °C. Then, 100 μL samples with an appropriate gradient were plated on LB solid media and incubated overnight in a constant temperature incubator at 36 ± 1 °C. Bacterial colonies with different sizes, colors and shapes were selected for purification to obtain pure bacteria. The obtained pure bacteria were inoculated into 3.5 mL of LB liquid media and incubated overnight on a constant temperature shaker at 36 ± 1 °C. One milliliter of fresh bacterial solution was stored in 30 % glycerol and stored in a − 80 °C ultralow temperature refrigerator. Two milliliters of fresh bacterial solution was used to extract bacterial DNA using a TIANamp Bacterial Genome DNA Extraction Kit (TIANGEN, Beijing, China) according to the manufacturer's instructions. Then, a NanoPhotometer®N60 spectrophotometer (IMPLEN, Germany) was used to determine the concentration and quality of DNA, and PCR amplification after concentrating the qualified DNA. The amplified PCR products were sent to Shenzhen BGI Co., Ltd., for PCR amplification sequencing, and the sequencing results were compared using the Nucleotide Basic Local Alignment Search Tool (BLAST) (http://www.ncbi.nlm.nih. gov/blast/) in the GenBank database.

2.3. DNA extraction and real-time quantitative PCR

Fifteen-milliliter samples were filtered through 0.22 μm hydrophilic membranes (50 mm in diameter) for DNA extraction. DNA was extracted from the aerosol samples using a DNeasy Power Soil DNA Isolation Kit™ (MOBIO, USA) according to the manufacturer's instructions. All DNA samples were checked for quantity and quality with a NanoPhotometer N60 spectrophotometer (IMPLEN, Germany) and stored at −20 °C for further analysis.

High-throughput quantitative PCR (HT-qPCR) was used to detect and quantify a total of 11 ARG subtypes and the intl1 and 16S rRNA genes. These ARG subtypes belong to five major classes of antibiotics that are frequently detected in the air, such as sulfonamides (e.g., sul1 and sul2); tetracyclines (e.g., tetA, tetC, and tetX); quinolones (e.g., qnrA and qnrB); macrolides (e.g., ermA and ermB); and β-lactams (e.g., ampC and OXA-1). Quantitative PCR (qPCR) analyses were performed using a Bio-Rad IQ5 instrument (Bio-Rad Company, USA) as previously described by Mao et al. (Mao et al., 2015). A total of 13 primer pairs are shown in Table S3, and the qPCR protocol used is shown in S1. The abundances of ARGs and MGE were normalized to the sampling volume.

2.4. 16S rRNA gene amplicon sequencing

DNA samples were sent to Novogene Biological Information Technology Co., Ltd. (Tianjin, China). The PCR conditions were as follows: initial denaturation at 98 °C for 2 min, followed by 30 cycles at 98 °C for 30 s, annealing at 50 °C for 30 s, and a final extension at 72 °C for 5 min. The PCR products were isolated by 2 % agar gel electrophoresis, and approximately 450 basis point fragments were purified using Agincourt Apure XP (Beckman Coulter Inc., CA) (Yang et al., 2019).

2.5. Minimum inhibitory concentrations of bacterial isolates

MICs were determined using the 96-well plate microdilution method to investigate the changes in antibiotic resistance during COVID-19 of the opportunistic pathogenic bacteria in the same isolates as shown in Table S4. A total of 13 antibiotics, including β-lactams (ampicillin (AMP), piperacillin (PIP), ceftazidime (CAZ), ceftriaxone (CRO), imipenem (IMP)); aminoglycosides (gentamicin (GEN)), quinolones (ciprofloxacin (CIP)); macrolides (erythromycin (ERY)); tetracyclines (tetracycline (TET)); polypeptides (polymyxin B (PB)); chloramphenicol (chloramphenicol (CL)); sulfonamides (sulfamethoxazole (SMZ)); and rifamycin (rifampin (RIP)), were used. Then, 100 μL of Mueller-Hinton broth was used as the carbon and energy source, and 100 μL of each bacterial suspension was mixed with antibiotic solution using serial dilutions and dispensed into each well of a microplate. After incubation for 16–18 h at 36 ± 1 °C (Zhao et al., 2021), the OD600 values of the 96-well plate were measured with an enzyme-labeled instrument (Synergy H4, BioTek, America).

2.6. Evolution of Bacillus cereus due to disinfectant exposure

Due to the high detection rate, toxicity, pathogenicity and enhance antibiotic resistance of bacillus cereus in aerosol samples after the COVID-19, B. cereus isolated before COVID-19 was used as the target strain. In the sampling area of this study, “84” and chlorine disinfectant are mainly used as outdoor disinfectants as shown in Table S2, and their main the active ingredient of both types of disinfectants is sodium hypochlorite (NaOCl). Therefore, “84” disinfectant was used to conduct an 8-day evolution experiment. Isolated B. cereus was plated on LB solid medium and placed in a constant temperature incubator (36 ± 1 °C) for overnight culture. “84” disinfectant was used and evenly sprayed on the cultured B. cereus solid plate and left to stand for 10 min. A swab scraper was then placed in 3.5 mL of LB liquid medium and placed in a shaker (36 ± 1 °C) for overnight culture. The next day, the bacterial solution was plated on LB solid medium, and the above experiments were repeated. The MICs of the 13 antibiotics for the evolved strains were measured at 0, 3 and 8 days (Ceragioli et al., 2010).

2.7. Data analysis

Data were analyzed using Microsoft Excel 2010 and Origin 2018. Heatmap and PCoA analyses were conducted using TBtools and R studio, respectively.

The exposure doses and human health risk assessments of ARGs were estimated based on models recommended by the U.S. EPA. The exposure mechanisms to airborne ARGs include skin contact and respiratory inhalation (Wang et al., 2019). The average daily dose (ADD) was calculated based on the following Eqs. (1), (2):

ADDrespiration=c×IR×EF×ETrespirationBW×AT (1)
ADDskin=c×sA×pc×EF×ETskin×24BW×AT (2)

where ADDrespiration and ADDskin represent the average exposure doses (copies/d/kg) from respiration inhalation and skin contact (copies/d/kg), respectively, c is the airborne ARG concentration (copies/m3), and EF is the exposure frequency (d/a). In Eq. (1), IR is the inhalation rate (m3/d) and ETrespiration is the respiratory inhalation exposure time (a). In Eq. (2), sA is the skin exposure surface area (m2), pc is the skin permeability (m/h), and ETskin is the skin contact exposure time (a). All parameters in Eqs. (1), (2) refer those used by the U.S. EPA (Yang et al., 2019) and are summarized in Table S5 and Table S6.

3. Results and discussion

3.1. Increased airborne ARG levels during COVID-19

ARG subtypes and abundances were quantified to examine the ARG variations before and during the COVID-19 period. Among the 11 ARG subtypes and intI1 that were frequently detected in the air, 5 ARGs and 1 MGE, including sulfonamide (sul1 and sul2), tetracycline (tetA and tetC), β-lactams (ampC) and MGE (intI1), were detected during the COVID-19 period. Quinolones (qnrA and qnrB), macrolides (ermA and ermB), β-lactams (OXA-1) and tetracyclines (tetX) were not detected. Overall, ARG subtypes were found to decrease after the COVID-19 pandemic (Fig. 1A). Previous studies reported similar observations (Zhang et al., 2015; Zhuang et al., 2015); as the chlorine concentrations increased, the ARG subtypes decreased, indicating that disinfection effectively decreased the diversity of ARGs. According to Dodd (2012), disinfection significantly reduces the total ARG amounts due to the direct degradation of extracellular and/or intracellular DNA.

Fig. 1.

Fig. 1

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Subtypes of antibiotic resistance genes (ARGs) and mobile genetic element (MGE) (A) and the absolute abundances of antibiotic resistance genes (ARGs) and mobile genetic element (MGE) (B) in the four functional areas before and during COVID-19, where “B” are samples taken before COVID-19, “D” are the samples obtained during COVID-19, “CA” is the commercial area, “EA” is the educational area, “RA” is the residential area, and “STP” is WWTPs.

Although the ARG subtypes decreased, this study found increased ARG abundances in airborne environments after the COVID-19 pandemic (Fig. 1B). Tetracycline resistance genes showed the highest relative abundances during the COVID-19 period, which were up to approximately 13-fold greater than before the COVID-19 period. In addition, the absolute abundances of both ARGs and intI1 increased in the four functional areas after the COVID-19 pandemic (Fig. S1). Among them, the absolute abundances of sul1 and sul2 in CA aerosols increased by approximately one order of magnitude, and the absolute abundances of tetA and tetC in EA increased by approximately one order of magnitude. Similar results were reported by Shi et al. (2013), in which ampC and tetA were enriched by disinfection. After disinfection, the abundances of tetracycline (tetA, tetB, and tetC); sulfanilamide (sul1, sul2 and sul3); β-lactam (ampC); rifampicin (katG) and vancomycin (vanA) increased significantly by up to 3.8-fold (Liu et al., 2018).

It has been well documented that tetracycline resistance genes are less susceptible to disinfection (Huang et al., 2013), and low chlorine concentrations are more likely to lead to enrichment of ARGs (Jutkina et al., 2018). It was speculated that chlorination may play a co-selective role in bacterial resistance. Another reason may be related to the possibility that insufficient chlorine dosages promote conjugative transfer, in which cell surfaces include more pili as the ARG transfer pathway. Additionally, the absolute abundance of intI1 increased significantly after the COVID-19 pandemic (Fig. S1F). It is well known that antibiotic resistance can be achieved through horizontal gene transfer (HGT) by MGEs (Mc Carlie et al., 2020). Integrons capture or transmit genes, such as integrons related to intI1 that transfer sul1 (Liao and Chen, 2018). Therefore, the extensive use of chlorinated disinfectants in public places during the COVID-19 period was likely to increase the abundances of ARGs in aerosols by affecting HGT mediated by intI1. These results indicated that ARGs were influenced by disinfection. These enriched ARGs can be harbored in bacteria and transferred horizontally to pathogens via MGEs, posing potential public health risks.

Urban aerosols accommodate rich and dynamic ARGs and MGEs, and emphasize the role of temperature and air quality in shaping the profile of ARGs (Zhou et al., 2023). In this study, the two sampling events both were conducted in September. Therefore, the temperature and air quality were similar as shown in Table S1. The use of disinfectants has generally increased after the outbreak of the epidemic, and so as to Shijiazhuang as shown in Table S2. It has been demonstrated that disinfection increases antibiotic resistance in bacteria (Zhang et al., 2017). Therefore, the use of disinfectants is considered to be an important reason for the increase of ARG abundance in aerosols after the COVID-19 pandemic.

3.2. Microbial community structures varied during COVID-19

The 16S rRNA absolute abundances were quantified to examine the total bacterial community before and during the COVID-19 period. As shown in Fig. 2A, aerosols harbored 1 order of magnitude lower levels of 16S rRNA total absolute abundances during the COVID-19 period than before. In the four functional areas, the absolute 16S rRNA abundances ranged from 106 to 107 during the COVID-19 period and 107 to 108 copies/m3 before the COVID-19 period (Fig. 2B). Similar to the trend of ARG abundance, we observed that the absolute abundance of aerosol-associated 16S rRNA genes was 1 orders higher in the before disinfection aerosols (3.8 × 107 copies/m3) than that of during (5.0 × 106 copies/m3) in our laboratory disinfection experiment (Fig. S2), which consistent with the results reported by Zhao et al. (2022). Similarly, the diversities and abundances of the bacterial communities decreased after long-term exposure to disinfectants (Tandukar et al., 2013). Chlorine-containing disinfectants were the most commonly used agents during the COVID-19 period and acted as widely nonspecific oxidants that inactivated bacteria by randomly destroying cellular components such as lipids, amino acids, and nucleic acids (Hora et al., 2020). Large-scale disinfection may have resulted in lower 16S rRNA abundances because most of the sensitive strains were inactivated by disinfectants.

Fig. 2.

Fig. 2

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The total absolute abundances of 16S rRNA (A) and absolute abundances of 16S rRNA in the four functional areas (B) before and during the COVID-19 pandemic.

As shown in Fig. 3 , the PCoA results showed that the compositions of bacterial community structures were significantly distinct after COVID-19 (p < 0.01). The bacterial communities were dominated by Proteobacteria among the top 10 most abundant phyla (Fig. S3). During the COVID-19 period, the relative abundance of Proteobacteria decreased by 3 %, while those of Firmicutes and Actinobacteria increased by 0.5 % and 5 %, respectively. (Fig. S3). Therefore, the variations in bacterial community structures at the phylum level were not significant after the COVID-19 epidemic. In other words, Proteobacteria persisted during the COVID-19 period. However, the research findings at the genus level showed that the predominant genus, Comamonas, decreased by 60 % after the COVID-19 pandemic. Escherichia, Stenotrophomonas, Pseudomonas, Acidovorax and Bacillus increased by 33 %, 15 %, 17 %, 14 %, and 0.03 %, respectively (Fig. 4A). Both Comamonas (e.g., Comamonas testosteroni) and Escherichia are common human pathogens. Infection by Comamonas testosteroni is not frequent, and fewer cases have been reported (Li et al., 2016). In total, the absolute abundances of opportunistic pathogens increased (Fig. S4). Disinfectant resistance genes have been detected in Escherichia (e.g., Escherichia coli) (Wassenaar et al., 2015). They are tolerant to high chlorine concentrations, indicating the influence of chlorination on shifts in bacterial communities.

Fig. 3.

Fig. 3

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PCoA of the bacterial communities before and during the COVID-19 pandemic.

Fig. 4.

Fig. 4

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Total relative abundances of the top 30 genera (A) and relative abundances of the top 30 genera in the four functional areas (B) before and during the COVID-19 pandemic, where “B” are the samples taken before the COVID-19 pandemic, “D” are samples taken during the COVID-19 pandemic, “CA” is the commercial area, “EA” is the educational area, “RA” is the residential area, and “STP” is WWTPs.

The bacterial genera compositions in the four functional areas were different during the COVID-19 period (Fig. 4B). Disinfectants reduced the absolute bacterial abundances in the four functional areas during the COVID-19 period. The absolute bacterial abundances in commercial areas decreased by approximately one order of magnitude (Fig. S5). The absolute abundances of Comamonas decreased by 1 order of magnitude in residential areas and WWTPs, while those of Escherichia increased by approximately one order of magnitude in WWTPs. The absolute abundances of the top 30 bacteria in commercial areas before the COVID-19 period were one order of magnitude higher than those in the other functional areas, which may have been caused by the substantial flow of people in commercial areas. Shijiazhuang Wanda Plaza was chosen as the commercial area in this study and has a superior geographical location and convenient transportation. Universities, hospitals, communities and parks are located nearby, and the crowds are dense and complex. Zhao et al. (2021) showed that the absolute abundances of indoor bacteria were higher than those of outdoor bacteria. After evaluating the correlations among bacteria in aerosols and environmental factors, it was found that the bacteria in the indoor aerosols were mainly positively correlated with relative humidity, air temperature and population density. Although the aerosol samples obtained from commercial areas in this study were collected outdoors, the population density was relatively higher, and the population changed greatly with large uncertainty factors. Therefore, this may be one of the reasons for the high bacterial abundances in the commercial area.

Increased ARG abundances and decreased bacterial abundances indicate increases in antibiotic-resistant bacteria and/or increased antibiotic resistance of bacteria during COVID-19 under the action of disinfectants, which may enhance the potential risks of opportunistic pathogens to human health. Long-term exposure to disinfectants can lead to enrichment of chlorine-resistant bacteria, mainly Pseudomonas (e.g., Pseudomonas aeruginosa). A previous study also illustrated that the abundances of Proteobacteria decreased, while those of Firmicutes, Actinobacteria, Pseudomonas and Bacillus increased (Jia et al., 2020). Because different species of bacteria have different sensitivities to disinfectants, it may be more difficult to inactivate gram-negative bacteria and Bacillus (Russell, 1999). Gram-negative bacteria have thin peptidoglycan cell walls and external lipopolysaccharide guarantee layers, which may provide additional barriers (Shang and Blatcheley, 2001). Moreover, bacterial phenotypic characteristics, such as slow growth and thick cell walls, also help bacteria to resist chlorine. Tandukar et al. (2013) suggested that as a result of long-term exposure to disinfectants, Proteobacteria and Bacteroidetes dominated microbial structures after exposure to disinfectants. Therefore, some chlorine-resistant bacteria persisted under the effect of large-scale disinfection during COVID-19, and thus, the compositions of bacterial community structures shifted.

3.3. Enhanced antibiotic resistance during COVID-19

Thirteen antibiotics were selected to analyze the resistance of human pathogens, including Bacillus cereus, Pseudomonas aeruginosa, Stenotrophomonas maltophilia and Staphylococcus hominis, which were isolated from aerosols before and during the COVID-19 period. Compared to the period before COVID-19, the resistance levels of four human pathogens increased, which was mainly manifested by increased resistance to β-lactam, polypeptide and macrolide antibiotics (Fig. 5 ). Bacillus cereus had the same resistance to CIP, GEN, CL and SMZ, and the resistance to the other nine antibiotics, namely, AMP, CAZ, CRO, PIP, IMP, PB, ERY, TET, and RIP, increased. Stenotrophomonas macinophilus showed increased resistance to AMP, CAZ, IMP, PB, ERY and GEN; Staphylococcus hominis exhibited increased resistance to AMP, CAZ, PIP, PB, ERY, and SMZ. Prior to COVID-19, three other bacteria were incredibly resistant to the antibiotics CL and SMZ, except for Staphylococcus hominis. Among them, the level of resistance of Pseudomonas aeruginosa and Stenotrophomonas macinophilus was not optimistic. The MIC values of CRO and PB against Bacillus cereus indicated antibiotic resistance as high as 512 mg/L during COVID-19; however, the corresponding antibiotic control groups against Staphylococcus hominis and Pseudomonas aeruginosa were as low as 4 mg/L and 1 mg/L. Pseudomonas aeruginosa showed increased resistance to CAZ, CRO, PIP, IMP, ERY, CIP, GEN, SMZ and RIP. During COVID-19, the MIC values of AMP, CRO, CL and SMZ against Pseudomonas aeruginosa reached 512 mg/L.

Fig. 5.

Fig. 5

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Bubble diagram showing the OD600 values and MICs of Bacillus cereus (B. cereus), Pseudomonas aeruginosa (P. aeruginosa), Stenotrophomonas macinophilus (S. macinophilus), and Staphylococcus hominis (S. hominis) bacteria isolated from the before and during the COVID-19 pandemic. The blank represents the negative control.

In total, the MIC of CRO and PB against B. cereus, AMP and CL against Pseudomonas aeruginosa and CL against Staphylococcus hominis reached 512 mg/L during the COVID-19 pandemic (Fig. 5). Sakagami et al. (1989) have shown that Pseudomonas aeruginosa can resist disinfectants by increasing the contents of phospholipids and neutral lipids in cell walls. Antibiotic resistance can be altered by altering naturally or horizontally transferred resistance genes, including those associated with bacteria exhibiting antibiotic resistance, such as drug degrading enzymes (β-lactamase), and those associated with bacterial membrane effluence pumps, such as OprR in Pseudomonas aeruginosa (Palmer et al., 2018). Kim et al. (2018) suggested that transcriptome sequencing of Pseudomonas aeruginosa exposed to high concentrations of benzalkonium chloride (BACs) showed that upregulation of drug efflux pump genes increased the rate of BAC excretion from cells. Efflux pump is the main mechanism of antibiotic resistance and disinfectant resistance. It is quite possible that disinfectant use has increased antibiotic resistance to human pathogens during COVID-19 due to the same resistance mechanism.

Due to the high detection rate, toxicity, pathogenicity and enhance antibiotic resistance of bacillus cereus in aerosol samples after the COVID-19, B. cereus isolated before COVID-19 was selected and used as the “84” disinfectant for the evolution experiment under exposure to disinfectant. With increasing exposure times, B. cereus showed increasing resistance trends to 10 antibiotics, including β-lactam, polypeptide, chloramphenicol, and tetracycline (Fig. 6 ). Similarly, a previous study also suggested that exposure to disinfectants increased the resistance of some gram-negative bacteria to antibiotics (e.g., sulfamethoxazole and ampicillin) (Kampf, 2018). The resistance mechanisms to penicillin and tetracycline both include efflux pump, membrane permeability and antibiotic enzyme modification, indicating that the resistance mechanisms of antibiotics and disinfectants have many common characteristics (Lin et al., 2016). Higher incidences of antibiotic-resistant bacteria have been reported in environments where disinfectants were infrequently used (Heir et al., 2001). Most likely, bacteria developed cross-resistance to disinfectants and antibiotics (Lin et al., 2016). This further suggests that large-scale spraying of disinfectants during COVID-19 can increase bacterial resistance in aerosols.

Fig. 6.

Fig. 6

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Increased antibiotic resistance of Bacillus cereus exposed to disinfectants, where “AMP” denotes “ampicillin”, “CAZ” denotes “ceftazidime”, “CRO” denotes “ceftriaxone”, “PIP” denotes “piperacillin”, “IMP” denotes “imipenem”, “PB” denotes “polymyxin B", “ERY” denotes “erythromycin”, “CIP” denotes “ciprofloxacin”, “GEN” denotes “gentamicin”, “CL” denotes “chloramphenicol”, “TET” denotes “tetracycline”, “SMZ” denotes “sulfamethoxazole” and “RIF” denotes “rifampin”.

The effects of disinfectants on bacteria mainly include changing the permeability of cell membrane, denaturing proteins or acting on the functional groups of enzymes in cells to change or inhibit their activities. In this study, the abundance of ARGs in bacteria aerosols increased (Section 3.1), and chlorine resistant bacteria became the main bacterial category after the COVID-19 pandemic (Section 3.2). In previous study, it was also found that there was a close correlation between the resistance of chlorine resistant bacteria to chlorine disinfectants and antibiotic resistance (Khan et al., 2016). On the one hand, bacterial individual cells, such as increasing the expression of efflux pump (Karumathil et al., 2014), and bacterial populations, such as triggering oxidative stress regulatory proteins (Jin et al., 2020), both can produce resistance to disinfectants. on the other hand, chlorine disinfection may affect the horizontal transfer of resistance genes through various ways, such as increasing the insertion sequence of resistance genes (Shi et al., 2013), the abundance of mobile genetic elements (Zhang et al., 2019a) and the permeability of cell membrane due to chlorine damage (Yu et al., 2016). Therefore, the use of chlorine disinfectants was an important reason for the increase of antibiotic resistance of bacteria, especially chlorine resistant bacteria.

3.4. Higher levels of human health risk during the COVID-19 pandemic

Disinfectants significantly promoted ARG abundances in the air during COVID-19, which may increase potential human health risks due to their high abundances in the air. In this study, the ADD model recommended by the U.S. EPA was used to evaluate the human health risks of ARGs due to disinfection during the COVID-19 pandemic (Wang et al., 2019). Respiratory and skin contact are the two main routes through which ARGs enter the body from exposure to air. According to the results shown in Fig. 7 , both respiratory and skin contact showed higher levels of exposure to ARGs during the COVID-19 pandemic than before. The respiratory intakes of ARGs during COVID-19 were 2.3 × 106 copies/d/kg for adult women, 2.6 × 106 copies/d/kg for adult men, and 5.4 × 106 copies/d/kg for children (Fig. 7A). The ARG intake doses received through breathing by adults during the COVID-19 pandemic were one order of magnitude higher than before, and the ARG intake doses received through breathing by children during COVID-19 were more than three times higher. Before COVID-19, the ARG doses were one order of magnitude higher in children than in adults, approximately 2.3 times higher in children than in adult women and 2.1 times higher in adult men. The respiratory intake levels of resistance genes were higher in adult males before and during COVID-19 than in adult females.

Fig. 7.

Fig. 7

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Total exposure doses by respiratory (A) and skin contact (B) of antibiotic resistance genes to humans before and during the COVID-19 pandemic.

According to the results shown in Fig. 7B, the doses due to skin contact exposure to resistance genes during COVID-19 were 7.5 × 102 copies/d/kg for adult women and 7.0 × 102 copies/d/kg for adult men. Children were exposed to resistance genes through the skin at a dose of 2.0 × 103 copies/d/kg. The doses of resistance genes received through the skin were higher in adults and were one order of magnitude higher in children during COVID-19 than before. During COVID-19, children were exposed to resistance gene doses through the skin that were approximately one order of magnitude higher than those for adults. Before COVID-19, children were exposed to ARGs through the skin that were approximately 2.6 times higher than those for adult women and 2.8 times higher than those for adult men. The ARG doses received from skin contact before and during COVID-19 in adult women were higher than those for adult men.

Overall, the exposure doses of ARGs via respiratory contact were much higher than those due to skin contact. Respiratory intake was the main route through which ARGs from air exposure entered the body. Furthermore, the exposure doses of ARGs through respiratory intake were highest in commercial areas, followed by WWTPs, residential areas and educational areas (Fig. 8 ). The inhalation levels of ARGs in commercial areas during COVID-19 were approximately one order of magnitude higher than those in the other functional areas, which may be related to the higher abundances of ARGs in commercial areas. Fig. 8 shows that the inhalation levels of ARGs in adults in commercial areas during COVID-19 were approximately one order of magnitude higher than before, and the inhalation of levels ARGs for children during COVID-19 were approximately three times higher than before. The ARG doses inhaled by children in commercial areas before COVID-19 were approximately one order of magnitude higher than those inhaled by adults, and the ARG doses inhaled by children during COVID-19 were more than two times greater than those inhaled by adults. Respiratory intake of ARGs in adult males was slightly higher than that in adult females before and during COVID-19 in commercial areas. The same trends among children, female and male adolescents were found in the other three functional areas.

Fig. 8.

Fig. 8

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Exposure doses of antibiotic resistance genes via the respiratory system in the four functional areas before and during the COVID-19 pandemic.

Respiratory resistance genes were more abundant in WWTPs than in educational areas and residential areas. There was a fecal-oral route and droplet transmission of SARS-CoV-2 (Arslan et al., 2020). During COVID-19, workers were still conducting management and operations, which involved droplets and direct contact with the possibility of aerosol inhalation in WWTPs (Wang et al., 2019), and the infestation strengths in WWTPs were increased to comply with water discharge standards, disinfectant dosing quantities increased, and measures such as chlorine and peracetic acid for sterilization were used. WWTPs are one of the main locations for the release and transmission of ARGs, and disinfectant use increases antibiotic resistance levels and risks to human health.

4. Conclusions

In this study, we summarized the characteristics of ARGs and changes in bacterial community structures in aerosols that resulted from disinfection during the COVID-19 pandemic. The main conclusions are as follows: (1) During the COVID-19 pandemic, exposure to disinfectants decreased the ARG subtypes, while their abundances significantly increased. That is, compared with the period before COVID-19, large-scale use of disinfectants increased antibiotic resistance levels during the COVID-19 pandemic. (2) Compared with the period before COVID-19, the 16S rRNA abundances of bacteria decreased significantly during the COVID-19 pandemic due to the large-scale use of disinfectants, the structures of the bacterial communities changed, and the levels of bacterial resistance increased. (3) Large-scale use of disinfectants increased the resistance of aerosol bacteria to antibiotics, and at the same time, human health risks were significantly higher, and children's health risks were higher than those of adults.

All in all, with the pandemic already in progress, this situation will gradually improve, but the great pressure from new cases still continues all around us; a post-pandemic era of normalized protection is particularly important, the use of antibiotics in daily life and disinfectants should also be considered, which may lead to a risk of cross-resistance, which would thus increase the risk of resistance and cause serious harm to human health. We should improve the protection and rational use of disinfectants, ensure that their use complies with the specifications, and use caution with the large-scale use of air disinfectants.

CRediT authorship contribution statement

Qing Wang: Conceptualization, Writing-original draft, Writing-Review &Editing.

Changzhen Liu: Writing-Review & Editing.

Shaojing Sun: Data curation, Writing- Original draft preparation.

Guang Yang: Visualization, Investigation.

Jinghui Luo: Data curation.

Na Wang: Data Curation.

Bin Chen: Visualization, Validation.

Litao Wang: Validation, Supervision, Conceptualization.

Declaration of competing interest

The authors declare no competing financial interest.

Acknowledgments

This work was supported by the National Natural Science Foundation of China (42077393), the National Natural Science Foundation of China (72091510), the Open Project of State Environmental Protection Key Laboratory of Pesticide Environmental Assessment and Pollution Control.

Editor: Ewa Korzeniewska

Footnotes

Appendix A

Supplementary data to this article can be found online at https://doi.org/10.1016/j.scitotenv.2023.162035.

Appendix A. Supplementary data

Supplementary material

mmc1.docx (1.2MB, docx)

Data availability

Data will be made available on request.

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Associated Data

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Supplementary Materials

Supplementary material

mmc1.docx (1.2MB, docx)

Data Availability Statement

Data will be made available on request.

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