Increased Indoor Exposure to Commonly Used Disinfectants during the COVID-19 Pandemic

Abstract

Quaternary ammonium compounds (QACs or “quats”) are a class of chemicals used as disinfectants in cleaning and other consumer products. While disinfection is recommended for maintaining a safe environment during the COVID-19 pandemic, the increased use of QACs is concerning as exposure to these compounds has been associated with adverse effects on reproductive and respiratory systems. We have determined the occurrence of 19 QACs in residential dust collected before and during the COVID-19 pandemic. QACs were detected in > 90% of the samples collected during the pandemic at concentrations ranging from 1.95–531 μg/g (n = 40, median 58.9 μg/g). The total QAC concentrations in these samples were significantly higher than in samples collected before the COVID-19 pandemic (p < 0.05; n = 21, median 36.3 μg/g). Higher QAC concentrations were found in households that have increased their cleaning routine during the pandemic and in those that generally disinfected more frequently (p < 0.05). Disinfecting products commonly used in these homes were analyzed and the QAC profiles in dust and in products were similar, suggesting that these products can be a significant source of QACs. Our findings indicate that indoor exposure to QACs is widespread and has increased during the pandemic.

Graphical Abstract

INTRODUCTION

The spread of the SARS coronavirus 2 (SARS-CoV-2), which causes the disease COVID19, has resulted in a surge in disinfectant use to keep household environments safe.^1,2 Intensified cleaning protocols during the COVID-19 pandemic specifically call for the increased use of disinfectants in homes and high-risk public spaces, such as schools, health and other care facilities, and food service and work spaces.

Disinfecting products containing quaternary ammonium compounds (QACs), also referred to as “quats”, are recommended by the United States Centers for Disease Control and Prevention (CDC) and Environmental Protection Agency (EPA) for disinfecting procedures specifically targeting the SARS-CoV-2.³ QACs are the major class of disinfectants and antimicrobials used in cleaning products, biocides, personal care products, and biomedical materials.^4,5 QACs are salts of quaternary ammonium cations with at least one long hydrophobic hydrocarbon chain substituent and other short-chain substituents, such as methyl or benzyl groups. The three most widely used QAC groups include benzylalkyldimethyl ammonium compounds (BACs, with C6–C18 alkylated chains), dialkyldimethyl ammonium compounds (DDACs, with C8–C18 alkylated chains), and alkyltrimethyl ammonium compounds (ATMACs, with C8–C18 alkylated chains) (Figure S1). Some QACs, including C12-BAC and C14-BAC, are classified by the EPA as high production volume chemicals based on the manufactured or imported amount exceeding 1 million pounds per year.² These compounds are able to disrupt the adipose cell membranes of living organisms and thus the viral envelopes and remove organic material. It is this property in particular that enables QACs to act as disinfectants and antimicrobials.⁶

Exposure to QACs has been associated with several adverse health effects. QACs are recognized as asthmagens, as previous animal and occupational studies have demonstrated that exposure to QACs may lead to a significant increase in asthma triggers and other breathing problems, such as pulmonary cell damage and inflammation.^7,8 Skin irritation and decreased fertility were observed in rodents and guinea pigs exposed to some QACs through inhalation and diet.^9–13 In addition, QACs increase the permeability of outer membranes of living organisms and their long-term use may disrupt the protective lipid membranes of the skin and potentially increase the absorption of toxic substances.¹⁴ Hence, the increased use of household disinfectants and other cleaning agents containing QACs during the COVID-19 pandemic is of significant concern.²

QACs have been detected in wastewater sludge, surface waters, sediments, and soil.^{5, 15–20} Moreover, high levels of QACs have been reported in fruits, food additives, milk, and other dairy products.^21–25 However, comprehensive studies on their occurrence in the indoor environment are lacking. Household dust has long been recognized as a reservoir and a major human exposure pathway for many environmental contaminants, especially for children.^26,27 Due to their low volatility, QACs are easily adsorbed to solid airborne particles and dust, where they are unlikely to degrade. This leads to long-term contamination of the indoor environment, which is likely to last long after the pandemic.²⁸ Therefore, a better understanding of the increased exposure to QACs during and after the COVID-19 pandemic is essential in order to assess its potential effects on human health.

This is the first study to investigate the occurrence of 19 QACs in residential dust collected before and during the outbreak of COVID-19. In addition, we also measured the levels of QACs in selected disinfecting products commonly used in sampled homes and evaluated the effects of using certain products and disinfection frequency on the levels of QACs in the indoor environment.

MATERIALS AND METHODS

Sample Collection and Analysis.

Forty dust samples were collected from residential homes in Indiana, United States in June 2020 (during the COVID-19 crisis in the United States). In addition, 21 dust samples collected from Indiana homes in 2018–2019 (before the COVID-19 outbreak) were obtained from the archives of the citizen-science program MapMyEnvironment. For both sample groups, dust from vacuum containers and bags (containing dust collected from the entire home) was transferred by the homeowner to resealable bags, delivered or shipped to the laboratory, and stored at room temperature until analysis. Information on the change of disinfecting habits (if disinfecting more frequently since the COVID-19 outbreak), on the disinfection frequency (how many times per month / week), and commonly used cleaning products in sampled homes was also collected at the time of sampling during the pandemic. Cleaning products (sprays and wipes) indicated as frequently used in homes sampled during the pandemic were purchased from local markets for analysis.

All dust samples were sieved using a 500 μm mesh size sieve, and approximately 100 mg of dust was transferred to a glass tube, spiked with a surrogate standard (d₇-C12-BAC), sonicated in 4 mL of acetonitrile for 1 hour, and centrifuged at 3000 rpm for 5 min. The supernatant was transferred into a clean tube and the residues were re-extracted with 4 mL of acetonitrile twice. The combined extracts were concentrated to 1 mL using nitrogen gas and spiked with an internal standard (d₇-C14-BAC) used for quantification of the target analytes. For the analysis of disinfecting products, 10 μL of a product was diluted with 9.99 mL acetonitrile, and then 1 mL of the diluted solution was spiked with the internal standard (d₇-C14-BAC) before the direct instrumental analysis.

The samples were analyzed using ultra-performance liquid chromatography-triplequadrupole mass spectrometry. The complete analyte list, details of the instrumental analysis, quality control and assurance measures, and data analysis are provided in the Supporting Information.

RESULTS AND DISCUSSIONS

Dust Concentrations.

Each of the 19 QACs was detected in > 90 % of the samples collected during the COVID-19 pandemic at μg/g concentration levels (Table 1). The total QAC concentration (∑QAC, the sum of 19 QACs) ranged from 1.95 to 531 μg/g (median 58.9 μg/g). Benzylalkyldimethyl ammonium compounds (BACs) were the major group of QACs found in dust at a median ∑BAC concentration (the sum of 7 BACs) of 27.1 μg/g. Dialkyldimethyl ammonium compounds (DDACs) and alkyltrimethyl ammonium compounds (ATMACs) were found at lower concentrations (median ∑DDAC [the sum of 6 DDACs] 12.3 μg/g and ∑ATMAC [the sum of 6 ATMACs] 8.78 μg/g). BACs, DDACs, and ATMACs accounted for 56, 26, and 18% of the ∑QAC concentrations, respectively. C12- and C14-BACs were the most abundant QACs, and contributed 29% and 22% to the ∑QAC concentrations, respectively. Among the DDACs and ATMACs, C10- and C18-DDACs and C16-ATMAC were the most abundant, respectively, and contributed up to 10% of the ∑QAC concentrations. Overall, these 5 compounds comprised about 80% of the ∑QAC concentrations. This high proportion is likely related to high production volumes and to the wide application of these individual QACs.¹⁵ Significant correlations were found among all QAC concentrations (Table S1), suggesting a common source for these compounds.

Table 1.

Detection frequencies (DF,%), minimum (min), maximum (max), and median concentrations (μg/g) of QACs in residential dust collected before (n = 21) and during (n = 40) the COVID-19 pandemic, contribution (contr, %) of each QAC to the ΣQAC concentrations, and percent change in concentrations measured in these two sample groups (based on median concentrations). MDL: method detection limit. The asterisks represent the statistical difference at p < 0.05 based on a Mann-Whitney test.

		Before the COVID-19				During the COVID-19					Change, %
QACs	DF	Min	Max	Median	Contr	DF	Min	Max	Median	Contr
BACs
C6-BAC	95	<MDL	0.015	0.00171	0.01	98	<MDL	0.084	0.004	0.01	134*
C8-BAC	100	0.0022	12.2	0.0496	0.2	100	0.0022	7.58	0.058	0.1	17
C10-BAC	100	0.0040	0.329	0.0213	0.1	100	0.0005	0.787	0.054	0.1	154*
C12-BAC	100	1.40	32.5	5.89	25	100	0.244	181	12.6	29	114*
C14-BAC	100	0.863	30.9	3.88	16	100	0.760	154	9.55	22	146*
C16-BAC	100	0.181	9.73	1.03	4.3	100	0.203	75.6	3.17	7.2	208*
C18-BAC	100	0.0393	6.07	0.431	1.8	100	0.061	34.8	1.16	2.6	169*
ΣBAC	100	3.19	74.2	14.2	48	100	1.66	421	27.1	56	91*
DDACs
C8-DDAC	100	0.056	7.33	1.10	4.6	100	0.0148	20.2	1.63	3.7	48
C10-DDAC	100	1.09	24.1	5.53	23	100	0.0219	32.8	4.30	10	−22
C12-DDAC	95	<MDL	0.139	0.0495	0.2	98	<MDL	2.91	0.047	0.1	−5
C14-DDAC	95	<MDL	0.050	0.0147	0.1	100	0.0002	0.462	0.016	0.04	9
C16-DDAC	100	0.0355	4.67	0.231	1.0	100	0.0031	4.24	0.374	0.9	62
C18-DDAC	100	0.0809	22.1	1.71	7.0	100	0.0192	33.1	3.47	7.9	103*
ΣDDAC	100	1.35	41.4	8.87	30	100	0.0595	68.9	12.3	26	39
ATMACs
C8-ATMAC	100	0.0007	0.253	0.0223	0.1	95	<MDL	0.507	0.057	0.1	156*
C10-ATMAC	100	0.0146	2.41	0.196	0.8	93	<MDL	6.76	0.266	0.6	36
C12-ATMAC	100	0.0166	22.5	0.758	3.2	100	0.0281	13.1	1.25	2.9	65
C14-ATMAC	95	<MDL	4.05	0.131	0.5	100	0.0034	2.51	0.275	0.6	110*
C16-ATMAC	100	0.246	14.0	2.20	9.3	100	0.0116	61.3	4.59	10	109*
C18-ATMAC	100	0.030	6.32	0.546	2.3	100	0.0096	9.80	0.841	1.9	54
ΣATMAC	100	0.698	26.1	6.36	22	100	0.235	66.5	8.78	18	38
ΣQAC	100	6.55	127	36.3	100	100	1.95	531	58.9	100	62*

Similarly, all QACs were detected in > 95% of the samples collected before the COVID-19 outbreak (Table 1), but at significantly lower concentrations than in samples collected during the pandemic (median 36.3 μg/g; p < 0.05, Figure 1A). Overall, the dust concentrations of 10 QACs have significantly increased during the pandemic compared to the dust collected pre-pandemic (Table 1). The median ∑QAC concentration in samples collected during the pandemic increased by 62% when compared to samples collected before the pandemic, with the highest increase of 91% found for BACs. Interestingly, the contributions of BACs, DDACs, and ATMACs to the ∑QAC concentrations (48, 30, and 22%, respectively) in pre-pandemic samples were similar to those found in dust collected during the pandemic, suggesting a similar source of QACs in both sample groups. These results indicate that the levels of QACs in the indoor environment have increased since the outbreak of COVID-19.

Figure 1.

The ∑QAC concentrations (μg/g) in dust collected from homes: A) during (n = 40) and before (n = 21) the COVID-19 pandemic; B) with increased (n = 29) and not changed (n = 11) disinfecting frequency during the COVID-19 pandemic; and C) more frequent (1–5 times per week; n = 27) and less frequent (less than once a week or do not use disinfecting chemicals; n = 13; three outliers were omitted) disinfecting. Concentrations are shown as boxplots, representing the 25^th and 75^th percentiles; black lines represent the median; and the whiskers represent the 10^th and 90^th percentiles. The asterisks represent the statistical difference at p < 0.05 based on a Mann-Whitney test.

When compared with the levels of other environmental contaminants reported in dust from the United States, the median QAC concentration in this study was about 3 times higher than that for organophosphate esters (16.8 μg/g)²⁶ and about 1,000 times higher than that for per- and polyfluoroalkyl substances (84.5 ng/g).²⁷ On the other hand, these QAC levels were about 6 times lower than those for phthalates (median 396 μg/g).²⁹ Incidentally, QACs were detected in urban estuarine sediment from New York, United States (median 29 μg/g)¹⁹ and in surface sediment from the Great Lakes (2.4 to 4.9 μg/g), but at lower concentrations than measured here.²⁰ These lower environmental levels may be due to the effectiveness of the removal processes at wastewater treatment plants.⁵

Concentrations in Cleaning Products.

Table S2 shows the QAC concentrations in 7 cleaning and disinfecting products indicated as commonly used in the homes that were sampled during the pandemic. All three QAC groups were detected in the analyzed products, but at widely varied concentrations. Products 1 and 2 had the highest ∑QAC levels, reaching 16,600 and 1350 mg/L and accounting for 1.66 % and 0.135 % by weight, respectively (similar to those indicated on the products’ labels, 1.2% and 0.18% by weight, respectively). These concentrations were 10–1000 times higher than those in the rest of the products (2.52–156 mg/L). BACs were the predominant compounds in Products 1–3, contributing 83, 99, and 98% to the ∑QAC concentrations (Figure S2). This contribution went down to 0.4–23% in Products 4–7. It should be noted that Products 1 and 2 are included in the EPA’s N list of disinfectants effective for the SARS-CoV-2.³⁰

The Effect of Disinfecting Practices.

Seventy-two percent of participants in this study indicated that they have increased the frequency of disinfecting in their homes since the beginning of the COVID-19 pandemic. Overall, the ∑QAC concentrations in homes with the increased disinfecting frequencies during the COVID-19 crisis (median 65.2 μg/g) were significantly higher than in homes that did not change their disinfecting routine (median 21.7 μg/g, p < 0.05) (Figure 1B and Table S3), suggesting that the intensified disinfecting practices can significantly increase exposure to QACs in the indoor environment.

The ∑QAC levels in homes that reported cleaning and disinfecting from one to few times a week were significantly higher than in homes that did not do weekly disinfecting or used disinfecting chemicals (p < 0.05, Figure 1C and Table S3). Overall, the homes with higher cleaning frequencies (1–5 times per week) had the ∑QAC concentration twice as high as homes with less frequent (< 1 per week or did not use disinfecting products) cleaning (medians 64.6 vs. 28.0 μg/g; p < 0.05). A linear regression between the average ∑QAC concentrations of the 10 QACs for which the levels have significantly increased since the COVID-19 outbreak (see Table 1) and the disinfecting frequency in homes was highly significant (r² = 0.9933, p = 00034, Figure S3), further indicating that the disinfecting practices can have a strong effect on the indoor QAC levels.

Ninety percent of households reported using a disinfecting product for their cleaning routine, and more than 80% of these households regularly used Products 1, 2, and 7. Figure 2 compares the average contributions of BACs, DDAC, and ATMACs in these three products and in dust samples from the homes that regularly used only these three products. These contributions in dust were similar to those in products (58, 24, and 18% vs. 64, 14, and 22%, respectively). The similarity between the profiles in dust and products suggests that disinfecting products frequently used in homes could be a significant source of these compounds.

Figure 2.

Comparison of the average contributions (%) of the three QAC groups to the ∑QAC concentrations in house dust and in the only three disinfecting products (Products 1, 2, and 7) used in more than 80% of the homes.

Exposure Assessment.

The estimated daily intakes (EDIs) of QACs during the COVID-19 pandemic via dust ingestion were calculated for toddlers and adults for the homes with higher disinfecting frequencies (1–5 times per week) and for the homes with less frequent cleaning (less than once a week) (Table 2). The highest ΣQAC EDI (615 ng/kg bw/day) was found for toddlers in homes with higher disinfecting frequencies and was up to 10 times higher than that estimated for adults. The EDIs for BACs and DDACs were below the tolerable daily intake thresholds for these two compound groups (1×10⁵ ng/kg bw/day) established by the European Food Safety Authority (EFSA).³¹

Table 2.

Estimated daily intakes (EDIs; ng/kg body weight [bw]/day) of each QAC group via dust ingestion for toddlers and adults in homes with more frequent (1–5 times per week) and less frequent (less than once a week or do not use disinfecting chemicals) disinfecting during the COVID-19 pandemic.

	More disinfecting		Less disinfecting
	Toddlers	Adults	Toddlers	Adults
ΣBAC	423	36.3	94.9	8.13
ΣDDAC	106	9.07	64.8	5.55
ΣATMAC	86.7	7.43	46.2	3.96
ΣQAC	615	52.7	206	17.6

Limitations and Implications.

This study had several limitations. The sample size was small for both dust and products due to the efforts to finish the study during the time period of the COVID-19 pandemic and the samples were collected from a limited geographic area. Dust was collected by citizen scientists from the vacuum bags and canisters due to the inability to enter the homes during the pandemic and it was not possible to determine which rooms were sampled. The samples collected before the COVID-19 pandemic were collected from different homes than those collected during the pandemic.

Nonetheless, this is the first study to assess human exposure to a wide suite of QACs in the indoor environment. The timing of this study is important considering the increased use of disinfectants due to the current COVID-19 pandemic. Our findings indicate that the indoor exposure to QACs is widespread and significantly higher in households with increased disinfecting frequencies due to the pandemic. The similarity between the profiles of QACs in products and dust collected from the same households suggests that the disinfecting products are a significant source of these compounds in homes. As the COVID-19 pandemic continues, the use of these compounds is expected to increase worldwide, and more research is needed to confirm our findings in other locations. Furthermore, more intense disinfecting procedures are advised for care facilities, schools, and other high-risk places, many of which serve populations most vulnerable to these exposures. Our findings call for urgent research on risks associated with the increased exposure to these chemicals.