Association of hand and arm disinfection with asthma control in U.S. nurses

Abstract

Objectives

To investigate the association between occupational exposure to disinfectants/antiseptics used for hand hygiene and asthma control in nurses.

Methods

In 2014, we invited female nurses with asthma drawn from the Nurses' Health Study II to complete two supplemental questionnaires on their occupation and asthma (cross-sectional study, response rate: 80%). Among 4,055 nurses (mean age: 59 years) with physician-diagnosed asthma and asthma medication use in the past year, we examined asthma control, as defined by the Asthma Control Test (ACT). Nurses were asked about the daily frequency of hand hygiene tasks: “wash/scrub hands with disinfectants/hand sanitizers” (hand hygiene) and “wash/scrub arms with disinfecting products” (surrogate of surgical hand/arm antisepsis). Analyses were adjusted for age, race, ethnicity, smoking status, and body mass index.

Results

Nurses with partly controlled asthma (ACT: 20-24, 50%) and poorly controlled asthma (ACT≤19, 18%) were compared to nurses with controlled asthma (ACT=25, 32%). In separate models, both hand and arm hygiene were associated with poorly controlled asthma. After mutual adjustment, only arm hygiene was associated with poorly controlled asthma: Odds Ratio [95%CI] for <1 time/day, 1.38[1.06-1.80]; ≥1 time/day, 1.96[1.52-2.51], vs. never. We observed a consistent dose-response relationship between frequency of arm hygiene tasks (never to >10 times/day) and poor asthma control. Associations persisted after further adjustment for surfaces/instruments disinfection tasks.

Conclusions

Frequency of hand/arm hygiene tasks in nurses was associated with poor asthma control. Results suggest an adverse effect of products used for surgical hand/arm antisepsis. This potential new occupational risk factor for asthma warrants further study.

Introduction

Healthcare workers have an increased risk of asthma, partly attributed to exposure to cleaning products and disinfectants [1,2]. Exposure to several agents used for cleaning/disinfection of surfaces and medical instruments (e.g., bleach, hydrogen peroxide, aldehydes, quaternary ammonium compounds), has been associated with increased risk of asthma and poor asthma control [1–3].

Hand hygiene practices in healthcare workers also involve chemical exposures. In hospitals, employees wash their hands 5-30 times per shift [4]. Products used for hand hygiene in U.S. healthcare are most often alcohol-based solutions [4,5]. For surgical personnel, hand antisepsis further involves washing/scrubbing their hands and forearms with water- or alcohol-based preparations generally containing chlorhexidine or povidone iodine [4,6,7].

The irritant and allergenic properties of antiseptic agents have been well-examined in relation to skin disorders [6]. In contrast, little is known regarding the potential respiratory risks associated with hand hygiene practices among healthcare workers. To address this question, we aimed to study the association between occupational exposures related to hand hygiene practices and asthma control in a large cohort of U.S. female nurses.

Methods

The Nurses' Health Study II (NHSII) began in 1989 with the inclusion of 116,430 female registered nurses from 15 U.S. states, aged 25–44 years. Follow-up questionnaires have been sent every 2 years since. In 2014-2015, all nurses who ever reported physician-diagnosed asthma in biennial questionnaires (1991-2015) and who recently returned a biennial questionnaire (2013 or 2015) were invited to complete two questionnaires, on their current occupation and on asthma (response rate: 80%). Details of data collection have been published elsewhere [3]. This investigation was approved by the Institutional Review Board at the Brigham and Women's Hospital (Boston, MA, USA).

Based on the asthma questionnaire, we selected participants who reiterated that a physician had diagnosed her as having asthma, and who reported use of asthma medication in the past year (asthma case definition). Asthma control was defined by the Asthma Control Test (ACT), based on activity limitations, frequency of symptoms, and frequency of use of quick-relief medication in the past four weeks [8].

In the occupational questionnaire, nurses were asked about the daily frequency of hand/arm hygiene tasks involving disinfectants (i.e., nurses were specifically asked not to include tasks only involving use of soap): “In your current job, how many times per day, on average, do you …”: “wash/scrub your hands with disinfectants or hand sanitizers” (later referred to as “hand hygiene”), to evaluate frequency of hand hygiene tasks; and “wash/scrub your arms with disinfecting products” (later referred to as “arm hygiene”), a surrogate to evaluate frequency of surgical hand/arm antisepsis [4]. Exposure to other disinfectants, i.e. used to clean surfaces/instruments, was evaluated by questionnaire and by a job-task-exposure matrix (JTEM) [9].

Associations between the frequency of hand and arm hygiene and asthma control were evaluated by multinomial logistic regressions adjusted for age, race, ethnicity, smoking status, and body mass index (BMI). Observations with missing values for covariates (all <1%) were excluded from multivariable analyses. Separate models were first used for each of the exposures of interest (hand / arm hygiene); then the two variables were entered in the same model for mutual adjustment. Additional models were further adjusted for exposure to disinfectants to clean surfaces/instruments. A two-sided P<0.05 was considered statistically significant. Analyses were run using SAS V.9 (SAS Institute, Cary, NC, USA).

Results

Among 4,237 nurses who returned both questionnaires on asthma and occupation, and who met our asthma case definition, participants with missing data for ACT (n=135) or for hand and arm hygiene tasks (n=47) were excluded. This yielded an analytic sample of 4,055 women. Participants were on average 59 years of age, 94% were white, 2% where Hispanic, 42% were obese (BMI≥30 kg/m2), 4% were current smokers and 29% were ex-smokers.

Reported frequency of hand hygiene tasks (never, 15%; <1 time/day, 4%; 1-3 times/day, 11%; 4-10 times/day, 24%; and >10 times/day, 46% - n=4,031) was higher than frequency of arm hygiene (never, 62%; <1 time/day, 17%; 1-3 times/day, 12%; 4-10 times/day, 5%; and >10 times/day, 4% - n=4,006). Thus, different cut-offs were chosen to classify exposure variables into three categories for hand hygiene (never, 15%; ≤10 times/day, 39%; and >10 times/day, 46%) and arm hygiene (never, 62%; <1 time/day, 17%; and ≥1 time/day, 21%). Among nurses who reported arm hygiene tasks ≥1 time/day, 78% reported hand hygiene tasks >10 times/day; among those who reported hand hygiene >10 times/day, 35% reported arm hygiene ≥1 time/day (table E1, online supplement).

In main analyses, nurses with partly controlled asthma (ACT 20-24, 50%) and poorly controlled asthma (ACT ≤19, 18%) were compared to nurses with controlled asthma (ACT =25, 32%). When using separate models for the two exposure variables, both hand hygiene (>10 times / day vs. never) and arm hygiene (≥1 time / day vs. never) were associated with partly and poorly controlled asthma (Figure 1A). Results were consistent when examining more detailed categories of asthma control (Table E2, online supplement). Moreover, similar associations persisted after further adjustment for other disinfection tasks: self-reported use of disinfectants to clean surfaces or medical instruments (Figure 1B; and Table E3, online supplement) or exposure to specific disinfectants evaluated by a JTEM (Table E4, online supplement).

Figure 1.

Associations of hand and arm hygiene with asthma control: (A) separate models for hand and arm hygiene; (B) separate models for hand and arm hygiene, with adjustment for self-reported weekly use of disinfectants to clean surfaces/instruments (no, surfaces only, instruments); and (C) hand and arm hygiene entered in the same model for mutual adjustment. Multinomial logistic regressions, adjusted for age, smoking status in 2013, body mass index in 2013, race and ethnicity. Results are presented as odds ratio and 95% confidence intervals (lines). Reference category was “never” for hand/arm hygiene and “controlled asthma” for asthma control.

However, after mutual adjustment (Figure 1C), only arm hygiene was associated with poorly controlled asthma: odds ratio [95% confidence interval] for <1 time/day vs. never, 1.38 [1.06-1.80]; and for ≥1 time/day vs. never, 1.96 [1.52-2.51]. Furthermore, among nurses who reported never doing arm hygiene tasks (n=2,443), no association was observed between hand hygiene and poor asthma control (>10 times / day vs. never, 1.10 [0.79-1.53]). In contrast, among nurses who reported infrequent hand hygiene (never or ≤10 times/ day, n=2,119), arm hygiene was associated with poorly controlled asthma (≥1 time/day vs. never, 2.59 [1.65-4.07]). Finally, when examining exposure frequency using more detailed categories (Figure E1, online supplement), we observed a consistent dose-response relationship between frequency of arm hygiene tasks (never to >10 times/day) and poor asthma control. This clear trend was not observed for hand hygiene.

Findings were confirmed for arm hygiene in sensitivity analyses using a more stringent asthma definition based on medication (Figure E2), and in models with further adjustment for nursing job types, household income, or husband's education (not shown). Moreover, the association between hand and arm hygiene and poor asthma control were similar in participants with or without allergy (defined by report of ever having had hay fever, seasonal allergy or allergic rhinitis; p_interaction for hand hygiene: 0.32; for arm hygiene: 0.29).

Discussion

In a study of 4,055 nurses with asthma, increased frequency of hand/arm hygiene tasks was associated with poor asthma control. The strongest evidence was found for an association between arm hygiene, a surrogate of surgical hand/arm antisepsis, and poor asthma control. This association remained statistically significant after adjustment for other disinfectant exposures and general hand hygiene tasks. It was further supported by a clear dose-response relationship across categories of arm hygiene tasks frequency.

To our knowledge, we are the first to report an association between hand hygiene tasks and adverse respiratory outcomes in healthcare workers. We used a validated asthma definition in this large population of nurses [10], and a standardized, validated, and commonly used measure of asthma control (ACT) which integrates several domains of the disease (symptoms, use of rescue therapy, sleep disorders, activity limitations) [8]. The main exposures of interest were evaluated by questionnaire. To reduce potential misclassification bias, we asked about frequency of hand hygiene tasks rather than use of specific agents (e.g., chlorhexidine), which may not be known by the nurses. Nonetheless, our results may be subject to differential misclassification bias (i.e., differential recall of exposure according to asthma control [11]). Although such bias cannot be completely ruled out, it would probably affect both exposures of interest similarly and lead to spurious associations for both hand and arm hygiene; however, after mutual adjustment, only frequency of arm hygiene was associated with poor asthma control. This pattern of associations is consistent with the hypothesis of an effect of agents specifically used for surgical hand/arm antisepsis, rather than regular hand hygiene products (alcohols). Latex exposure may be a cause of occupational asthma in healthcare workers. However, preventive efforts in the past decade, such as reduction in the use of powdered latex gloves, have led to a reduction of occupational asthma cases due to latex [12]. As reported earlier [3], use of latex gloves was not associated with poor asthma control in NHSII nurses, and is unlikely a confounder in the current study.

Limitations of the current study include its cross-sectional design, and the absence of information regarding the specific agents used for hand/arm hygiene tasks or test for sensitization to workplace agents. We are thus limited in drawing conclusions regarding potential agent(s) responsible for the observed association. However, chlorhexidine and povidone iodine are currently the agents the most commonly used for surgical hand/arm antisepsis [7]. Moreover, in a survey of a sample of the hospitals where NHSII nurses work, a chlorhexidine solution was used for surgical hand/arm antisepsis in 7 out of 8 hospitals surveyed [13]. Chlorhexidine is a skin sensitizer [6], and cases of occupational asthma or occupational airway allergy due to chlorhexidine have been reported in nurses [14]. Povidone-iodine also has been involved in skin allergies, although such cases are thought to be rare [6]. Beside allergenic potential, chlorhexidine and povidone iodine have well-documented skin irritation properties [6] and may also cause airway irritation [15]. Thus, mechanisms for a potential impact of antiseptic agents on respiratory health may include both sensitization and irritation, either through the dermal or inhalation route of exposure [16].

In conclusion, increased frequency of hand and arm hygiene tasks in nurses was associated with poor asthma control. Results suggest a role of products used for surgical hand/arm antisepsis, but not of common hand hygiene tasks. The potential respiratory risks of products used for hand hygiene merit further investigation, to confirm our results and to clarify the putative agents and mechanisms. If our findings are confirmed, hand hygiene tasks (and the identified hygiene products) would need to be added to current strategies of occupational illness prevention among healthcare workers, which may require the development of new approaches to maintain infection control standards in healthcare settings [17].

What this paper adds.

What is already known about this subject?

Healthcare workers have an increased risk of asthma, partly attributed to agents used for cleaning/disinfection of surfaces and medical instruments. However, little is known regarding the potential respiratory risks associated with disinfectants/antiseptics used for hand hygiene.

What are the new findings?

In a cross-sectional study of more than 4,000 U.S. nurses with asthma, we found that frequency of hand and arm hygiene tasks was associated with poor asthma control. Results suggest an adverse effect of products used for surgical hand/arm antisepsis.

How might this impact on policy or clinical practice in the foreseeable future?

If our findings are confirmed, some hand/arm hygiene tasks and the identified hygiene products would need to be added to current strategies of occupational illness prevention among healthcare workers.