Cleaning and disinfectant products are used widely in healthcare settings to minimize healthcareacquired infections (HAIs). HAIs among patients in US hospitals are estimated to have direct medical costs of at least $28.4 billion annually, and indirect costs to society of $12.4 billion due to early deaths and lost productivity.¹ Consequently, demand has increased for effective cleaning and disinfection products that can reduce infectious bacteria like methicillin-resistant Staphylococcus aureus (MRSA), vancomycin-resistant Enterococcus (VRE), and Clostridium difficile (C. diff) in healthcare environments in an effort to reduce costly HAIs.² Further, intensified cleaning protocols during the COVID-19 pandemic also contributed to increased demand for effective cleaning and disinfection products.³ Concerns about C. diff spores specifically, and HAIs from C. diff that cost the healthcare industry $1–5 billion annually, have led to increased demand for cleaning and disinfecting products with sporicidal activity.⁴ Sporicidal products composed of chlorine compounds, or mixtures of hydrogen peroxide (HP) and peroxy acids, are often used as surface cleaners and disinfectants in all areas of healthcare facilities.^2,5,6 Sporicidal products containing a mixture of HP, peracetic acid (PAA), and acetic acid (AA) have gained popularity in the last decade as a surface cleaner in healthcare settings due to their rapid-acting disinfectant properties and purported minimal damage to surfaces with no residual salts or films.⁷

Previous studies observed an increased risk for dermatitis, work-related rhinitis, work-related asthma, and chronic obstructive pulmonary disease (COPD) in workers exposed to cleaning and disinfectant chemicals in many different occupational settings.^8–16 Healthcare workers can potentially be exposed to high levels of many different cleaning and disinfecting products.^17–20 Many cleaning and disinfection products used in healthcare settings contain asthmagens, and the use of bleach, quaternary ammonium compounds, ammonia, spray cleaning products, and HP and PAA mixtures have been associated with asthma and respiratory symptoms among healthcare workers.^{12,13,21–25} Additionally, the recent increase in cleaning and disinfection product use associated with the outbreak of COVID-19 infections resulted in an increase in uncontrolled asthma among adults with current asthma.²⁶ Further, a recent longitudinal study of US nurses observed an association between exposure to disinfectants and COPD and suggested that regular use of chemical disinfectants among healthcare workers might be a risk for COPD.¹⁵ Although respiratory effects are well documented in healthcare workers exposed to cleaning and disinfecting products, few studies have evaluated quantitative exposures and the levels at which adverse health effects occur.

Despite widespread use of products containing a mixture of HP, PAA, and AA among U.S. hospitals, only a few assessments of hospital workers’ exposure to HP, PAA, and AA have been performed to date.^27,28 The objectives of this study were to evaluate healthcare workers’ (i) full-shift personal exposures to cleaning and disinfectant chemicals and work-related upper and lower airway symptoms reported during the shift, and (ii) departmental exposures to cleaning and disinfectant chemicals and work-related upper and lower airway symptoms in the previous 4 weeks.

Few studies have assessed occupational exposure to HP, PAA, and AA and health outcomes among workers in a healthcare setting.^27,28 In this study, and in a previous study at another multispecialty hospital, we observed health effects among hospital staff at exposure levels below established occupational exposure limits.²⁸ Exposures to HP (<3–559 ppb HP), PAA (<0.2–28 ppb PAA), and AA (<5–915 ppb AA) were similar to exposures measured in a previous study at another hospital where Product A was also used widely throughout the hospital, with exposures in the previous study measuring from <11 to 511 ppb HP, <2.2 to 48 ppb PAA, and <8.8 to 319 ppb AA. Both HP and PAA are strong oxidants, and the mixture of these strong oxidants potentially contributed to eye, upper airway, and lower airway symptoms reported by cleaning staff at relatively low levels of measured exposures.

In our current study, hospital staff using the product containing HP, PAA, and AA, or working in areas where the product containing HP, PAA, and AA was used, reported work-related upper and lower airway symptoms occurring during their shift and in the previous 4 weeks. Work-related eye irritation, nasal irritation, and wheeze during the shift or in the previous 4 weeks, as well as acute work-related shortness of breath was associated with exposure to the OM, or TM mixture of vapors from Product A. Similarly, increasing departmental P95 exposures, a surrogate for peak exposures, for the OM and TM were associated with significant increases in nasal irritation, eye irritation, and wheeze. Increasing departmental P95 exposures to HP and PAA were also associated with significant increases in nasal irritation (P95 PAA), sneeze (P95 PAA), eye irritation (P95 HP and P95 PAA), wheeze (P95 HP), chest tightness (P95 PAA), and shortness of breath (P95 HP). Our results demonstrate that exposure to vapors from the sporicidal product containing HP, PAA, and AA contributed to acute work-related eye, upper airway, and lower airway symptoms as well as work-related eye, upper airway, and lower airway symptoms in the previous 4 weeks in hospital staff.

Overall, nasal and eye irritation were the most commonly reported work-related symptoms among hospital staff in the present study. Occupational upper respiratory disease such as allergic rhinitis (hay fever, nasal allergies) and sinusitis is often more prevalent than occupational asthma.³⁸ Further, several studies indicate that rhinosinusitis might precede or occur with lower respiratory symptoms and asthma.^38–42 Additionally, the common airway hypothesis suggests that occupational upper airway disease indicates a risk for lower airway involvement, and upper respiratory involvement such as rhinitis or sinusitis can result in suboptimal control of asthma.^43–46 Despite associations between occupational rhinosinusitis and occupational asthma, occupational upper airway disease is often not considered serious.⁴⁶ In the present study, almost three-quarters of (74%) participants who reported acute work-related lower respiratory symptoms also reported acute work-related nasal symptoms and three-quarters (76%) of participants who reported work-related lower respiratory symptoms in the previous 4 weeks also reported work-related nasal symptoms in the previous 4 weeks, indicating an overlap between work-related nasal symptoms and work-related lower respiratory symptoms.

Our observation of significant associations between acute work-related eye irritation, nasal irritation, wheeze, and shortness of breath and exposure to the OM and TM is similar to results in our previous study of hospital cleaning staff using the same sporicidal product at another hospital²⁸; however, in that study we were unable to fully explore associations between exposures and cross-shift lower airway symptoms because the sample size and number of workers reporting acute cross-shift lower airway symptoms was too small to reliably calculate prevalence ratios for lower airway symptoms. We were able to assess chronic (usual or previous 12 months) symptoms however, and we observed significant associations between chronic shortness of breath on level ground and increases in exposure to the OM and TM, similar to our observation in this study of increases in acute work-related shortness of breath and exposure to the OM and TM. We also observed in this study that increases in chronic (previous 4 weeks) wheeze and chest tightness with increasing exposure to HP, PAA, OM, or the TM, which we did not observe in our previous study; however, previously we observed associations that approached significance for wheeze in the previous 12 months and increases in HP exposure. The larger sample size in the current study may have contributed to our ability to detect additional significant positive associations between exposures to vapors from the sporicidal product and lower airway symptoms.

Significant increases in nasal irritation, wheeze, chest tightness, and shortness of breath symptoms reported by hospital staff in our study are consistent with previous studies that have reported an increased risk for work-related rhinitis and asthma in workers exposed to cleaning and disinfectant chemicals.^8,10,47,48 Additionally, several case studies have reported occupational asthma caused by exposure to the mixture of HP and PAA and the Association of Occupational and Environmental Clinics (AOEC) listed this sporicidal product as an asthmagen in 2015.^23,24,49 Although the prevalence of current asthma in this study (7%) is lower than prevalence reported in other healthcare studies, we did observe significant associations between increasing exposure to vapors from the sporicidal product and acute work-related wheeze and shortness of breath, as well as chronic (previous 4 weeks) work-related wheeze, chest tightness, and shortness of breath.

Due to sampling limitations, we were unable to directly assess short-duration or peak exposures. However, we were able to utilize the departmental P95 as a surrogate for increased exposure intensity. The departmental P95 was used as a surrogate for exposure intensity because it captures exposure variability and short-duration high intensity exposures will contribute to higher full-shift exposures and greater variability. Similar significant associations were observed between departmental average and P95 exposures and symptoms in the previous 4 weeks, however odds ratios for upper and lower airway symptoms were larger with departmental P95 PAA exposure compared with departmental AM PAA exposure, suggesting that greater intensity in PAA exposures contributed to higher ORs for airway symptoms. Additionally, departmental P95 HP exposure was associated with significant increases in shortness of breath in the previous 4 weeks while departmental average HP exposure was not, suggesting that greater intensity in HP exposures contributed to shortness of breath in the previous 4 weeks. Our observation of significant associations between P95 exposures and upper and lower airway symptoms indicate a need to mitigate exposure intensity to the oxidant vapors (HP and PAA) in the sporicidal product.

The CDC’s Guideline for Disinfection and Sterilization in Healthcare Facilities acknowledges that irritant and allergic effects can occur with disinfectant chemical air concentrations at levels below OSHA or NIOSH exposure limits.⁵⁰ The Healthcare Infection Control Practices Advisory Committee (HICPAC) recommends that controls be used to minimize exposure to disinfectants, including elimination or substitution of the chemical, engineering or administrative controls, or the use of PPE.⁵⁰ We observed some cleaning staff using surgical masks or N95 respirators for the purpose of respiratory protection while dispensing or working with cleaning products; however, these types of masks are not appropriate respiratory protection while working with products that release gases or chemical vapors. As described previously, substitution with a low-level disinfectant for routine cleaning of surfaces in nonpatient areas is one option for reducing exposures; however, this might not be possible for surfaces in areas with isolation precautions in place and substitution with another low-level disinfectant containing phenolic, iodophors, alcohols, or chlorine compounds can also potentially cause upper airway irritation and asthma in exposed workers.²⁸ As Dumas et al. highlight in their recent study of COPD among US nurses exposed to disinfectants, additional studies are needed to investigate potential safer alternatives such as non-chemical means of disinfection such as steam or ultraviolet light.¹⁵ Where substitution with less hazardous cleaning products or nonchemical alternatives is not possible, engineering, administrative, and appropriate PPE controls can be used to mitigate exposure to HP, PAA, and AA.

Recent studies indicate the irritant characteristics of many chemicals found in cleaning and disinfection products can potentially contribute to a range of respiratory effects, including lower airway disease.¹⁵ Studies in the last decade have reported an increased risk of COPD, accelerated lung function decline, and higher rates of COPD deaths among cleaning workers.^51–53 Additionally, occupational exposure to cleaning products and disinfectants was recently associated with an increased risk for developing COPD.¹⁵ Our health survey was cross-sectional and limited to reported symptoms. Although in our study only five workers (7%) reported current asthma and only six workers (9%) reported chronic bronchitis (a form of COPD), significant associations were observed between exposure to vapors from the sporicidal product and lower airway symptoms commonly observed in asthma or COPD including shortness of breath, wheeze, and chest tightness.⁵⁴ However, our study did not include diagnostic tests such as pulmonary function tests, chest radiographs, or CT scans, limiting our ability to characterize respiratory function among the exposed workers.

Our study, although larger than our previous study of hospital cleaning staff using the same sporicidal product, was small and this could have limited our ability to detect additional significant associations among reported symptoms and exposures to HP, PAA, AA, the OM, and TM. Another limitation of our study is that we only collected full-shift TWA samples for the three chemical constituents, HP, PAA, and AA, found in Product A. Sampling and analytical limitations inhibited our ability to assess short-term exposures and compare short-term exposures with short-term exposure limits established by the ACGIH. Additionally, practical considerations limit the number of samplers a participant can wear during sampling; thus, personal samples were limited to samplers collecting samples for HP, PAA, and AA. However, we were able to record hospital staff’s use of other products containing sensitizers and irritants and observed that use of products containing sensitizers and irritants during a worker’s shift was significantly associated with acute work-related nasal irritation, sneeze, and difficulty breathing. Additionally, use of products containing sensitizers and irritants in the previous 4 weeks was significantly associated with difficulty breathing in the previous 4 weeks. We adjusted for use of products containing sensitizers and irritants during a worker’s shift or in the previous 4 weeks in our models that assessed associations between work-related symptoms and exposure to HP, PAA, AA, the OM, or TM. Another limitation of our study was that PPE use was not systematically measured. Thus, we were unable to assess whether voluntary use of goggles, surgical masks, or N95 respirators affected acute or chronic work-related symptom prevalence. An additional limitation is that sampling and analytical limitations hindered our ability to assess short-term exposures and compare short-term exposures with the established short-term exposure limits established by the ACGIH. Additionally, there was no validated method for full-shift sampling and analysis of PAA at the time of our survey. The sampling method we used to collect HP and PAA utilizes a sampling train that simultaneously collects HP and PAA.²⁹ We described the limitations of this sampling method previously.²⁸ Briefly, previous studies have indicated the potential for small amounts of PAA (3%) to be collected on the quartz filter used for collection and analysis of HP.⁵⁵ However, Christensen et al. acknowledge that this effect was minimized when the flow rate is maintained at 1 L/min, which is the flow rate used for our sampling. Small amounts of PAA could potentially have been misclassified as HP on the quartz filter. Thus, some of the associations we observed between exposure to HP and eye and airway symptoms could have been affected by a small misclassification of PAA as HP. Regardless, we attempted to address this potential limitation by summing values of relative HP and PAA concentrations to generate the OM and TM exposure variables used for all analyses.

Although our current and previous studies of occupational exposure to HP, PAA, and AA were limited to healthcare settings, the mixture of HP, PAA, and AA has broad application in other occupational settings outside of healthcare, including food production, agricultural, childcare, and food service industries. Additional studies are needed to 1) develop an improved sampling method for simultaneous HP and PAA collection and analysis, especially in settings where concentrations are anticipated to be relatively low and feasibility of short-term sampling is constrained by detection limits, and 2) characterize the potential eye and respiratory health effects from both acute and chronic occupational exposure to HP, PAA, and AA, across a wide range of potential exposures and occupational settings. Additionally, further study of alternative disinfection technologies is needed to identify potentially safer nonchemical technologies that can be used for infection control in healthcare settings.

Hospital workers exposed to HP, PAA, and AA reported acute work-related eye, upper airway, and lower airway symptoms at low levels of measured exposure. Increased exposure to the mixture of the two oxidants, HP and PAA, as well as the TM of HP, PAA, and AA, were significantly associated with increases in work-related acute and chronic eye and nasal irritation, wheeze, and shortness of breath. Additionally, increased departmental P95 exposures to vapors from the sporicidal product were associated with eye and nasal irritation, sneeze, wheeze, chest tightness, and shortness of breath. Further, associations between P95 exposures and upper and lower airway symptoms indicate a need to measure short-term exposures potentially contributing to elevated P95 exposures to inform more targeted exposure mitigation efforts. Our observations of work-related upper and lower airway symptoms among hospital workers exposed to vapors from a sporicidal product containing HP, PAA, and AA indicate a need for a combination of engineering, administrative, and PPE controls to reduce exposure. Additional studies are needed to investigate potentially safer nonchemical disinfection technologies as a means to simultaneously reduce healthcare workers’ exposure to disinfectants while also meeting the goal of infection control and minimizing costly HAIs.