Face Mask Use and Persistence of Livestock-associated Staphylococcus aureus Nasal Carriage among Industrial Hog Operation Workers and Household Contacts, USA

Background: Industrial hog operation (IHO) workers may persistently carry antibiotic-resistant, livestock-associated Staphylococcus aureus in their nasal cavities. It is unclear whether IHO work activities can alter IHO workers’ and their household members’ exposure to these bacteria. Objective: Our objective was to investigate the relationship of IHO work activities with persistence of antibiotic-resistant, livestock-associated S. aureus nasal carriage among IHO workers and their household members. Methods: At biweekly intervals over 4 months, IHO workers and their household members completed questionnaires and provided nasal swabs that were assessed for S. aureus, multidrug-resistant S. aureus (MDRSA), and livestock-associated markers (tetracycline resistance, scn absence, spa type). We examined the association between transient and habitual IHO work activities and S. aureus nasal carriage outcomes. Results: One hundred one IHO workers and 79 household members completed 1,456 study visits. Face mask use (each 25% increase) was associated with reduced odds of nasal carriage of MDRSA (odds ratio [OR]: 0.65 [95% confidence interval (CI): 0.46, 0.92], tetracycline-resistant S. aureus [OR = 0.74 (95% CI: 0.56, 0.97)], and S. aureus clonal complex (CC) 398/CC9 [OR = 0.77 (95% CI: 0.60, 0.99)]. IHO workers who ever (vs. never) gave pigs injections had higher odds of these outcomes. Among household members, living with an IHO worker who consistently (≥80% of the time) versus sometimes or never used a face mask was associated with reduced odds of carrying scn-negative S. aureus, tetracycline-resistant S. aureus, and S. aureus CC398/CC9 (OR range: 0.12–0.20, all p<0.05), and consistent IHO worker coveralls use was associated with reduced odds of household member MDRSA carriage only. Living with an IHO worker who habitually had contact with ≥4,000 hogs (vs. <4000) was associated with higher odds of household member livestock-associated S. aureus carriage. Conclusions: Consistent face mask use was associated with reduced exposure to antibiotic-resistant, livestock-associated S. aureus among IHO workers and their household members. https://doi.org/10.1289/EHP3453

. Antibiotics used for susceptibility testing of Staphylococcus aureus isolates. Table S2. Habitual occupational activities among 101 industrial hog operation (IHO) workers measured at biweekly intervals over four months, North Carolina, USA, 2013-2014. Table S3. Comparisons between crude and adjusted odds ratios for associations between 101 industrial hog operation (IHO) workers' time-varying (transient) personal protective equipment (PPE) use the week prior to biweekly nasal swabbing time points and changes in nasal carriage of multidrug-resistant and livestock-associated Staphylococcus aureus outcomes over four months, North Carolina, USA, 2013-2014.            75 (74) Note. IHO = industrial hog operation. IHO workers reported their occupational activities during the week prior at up to eight biweekly study visits. For binary exposures (e.g. handled dead pigs) expressed as "Sometimes or never" or "Consistently," "Sometimes or never" refers to activities that an IHO worker reported at ≥0 but <80% of completed biweekly visits, and "Consistently" refers to activities reported at ≥80% of completed biweekly visits. For continuous exposures (e.g. frequency of face mask use) expressed as "Sometimes or never" or "Consistently," "Sometimes or never" refers to activities that an IHO worker reported doing <80% of the time, on average, and "Consistently" refers to activities a worker reported doing ≥80% of the time, on average, across all completed biweekly visits. a For continuous occupational activities expressed as binary categories, the cut-off is the median value of the average numbers reported by workers over the four-month period, rounded to one significant digit. aOR were adjusted for time-varying changes in reported dust, temperature, and malodor levels, which were reported at 651/801 biweekly study visits completed by IHO workers. Dustiness inside the barn was reported on a Likert scale of 0-4, with 0=could see clearly and 4=could not see clearly. Barn temperature was reported on a Likert scale of 0-2, with 0=cold, 1=comfortable and 2=hot. Amount of malodor inside the barn was reported on a Likert scale of 0-4, with 0=no malodor and 4=extreme malodor. PR=prevalence ratio. CI=confidence interval. Individuals with no swabs positive for an outcome were defined as noncarriers of that outcome. Individuals with >0% and <80% of swabs positive for an outcome were intermittent carriers. Individuals with ≥80% of swabs positive for an outcome were persistent carriers. a Unadjusted prevalence ratios were generated using log binomial regression models using a generalized estimating equation (GEE) with an exchangeable correlation matrix to account for the non-independence of observations within households. Household members were the referent group. Stable measurements could not be produced for some associations due to small numbers. b

Supplementary Tables
The Rao-Scott chi-square test was used to examine the hypothesis that the distribution of non-carriers, intermittent carriers, and persistent carriers did not differ between industrial hog operation workers and household contacts for each outcome, while adjusting for within-household clustering. Degrees of freedom=2 for all tests. * = chi-square test could not be computed because at least one cell had a frequency of 0. 1.04(0.75,1.45) Note. IHO = industrial hog operation. OR = odds ratio. CI = confidence interval. SD=Standard Deviation. Effect measures were generated using conditional fixed-effects logistic regression models. Fixed effects models examine associations between within-person changes in an exposure and within-person changes in an outcome over time. a For binary exposures, the number of study visits for which the exposure was reported is provided as a percentage of all biweekly study visits, and as a percentage of the biweekly visits at which workers carried scn-positive S. aureus. For continuous exposures, the mean and standard deviation of the reported exposure is provided across all biweekly study visits and for biweekly visits at which participants carried scn-positive S. aureus. b Exposure was log-transformed for analysis. c Examined in increments of 25%. d Examined in increments of 10 hours. Note: IHO=Industrial hog operation. OR=Odds Ratio. CI=95% Confidence Interval. Odds ratio effect measures were estimated using logistic regression models with a generalized estimating equation and an exchangeable correlation matrix to account for the non-independence of observations within the same household. ORs were adjusted for the age and sex of household members. a IHO workers living in the household reported their occupational activities during the week prior at up to eight biweekly study visits. For dichotomous exposures expressed as "Sometimes or never" or "Consistently" (e.g. handled dead pigs), "Sometimes or never" refers to activities that an IHO worker reported at ≥0 but <80% of completed biweekly visits, and "Consistently" refers to activities reported at ≥80% of completed biweekly visits. For continuous exposures expressed as "Sometimes or never" or "Consistently" (e.g. percent time used face mask), "Sometimes or Never" refers to activities a worker reported doing ≥0 but <80% of the time, on average, across all completed biweekly visits, and "Consistently" refers to activities a worker reported doing ≥80% of the time, on average, across all completed biweekly visits. b Cut-off is the median value of the average numbers reported by workers over the four-month period, rounded to one significant digit.  Note: BL=Baseline study visit. NT=Non-typeable by spa typing. Biweekly sampling time points indicated by study visit columns 1-8. Boxes with text (either spa type or "NT") indicate S. aureus-positive sampling time points. White boxes without text indicate S. aureus-negative sampling points. Gray boxes indicate missing data (nasal swabs not collected or not analyzed). Boxes highlighted in black indicate spa types that have previously been associated with clonal complexes (CC) 398 or 9 in the literature. Figure S3. Temporal distribution of multidrug-resistant and livestock-associated Staphylococcus aureus nasal carriage outcomes among 101 industrial hog operation (IHO) workers at biweekly sampling intervals over four months, stratified by reported protective face mask usage of the IHO worker, North Carolina, USA, 2013-2014.
Note. BL = baseline study visit sampling time point. Biweekly sampling time points indicated by study visit columns 1-8. Black boxes indicate sampling points that were positive for the outcome indicated. White boxes without text indicate sampling time points that were negative for the indicated outcome. Grey boxes indicate missing data (nasal swabs not collected or not analyzed). OR=odds ratio. CI=confidence interval. a IHO workers who reported wearing a face mask <80% of the time during the week prior to nasal swabbing, on average, across all completed biweekly study visits. b IHO workers who reported wearing a face mask ≥80% of the time during the week prior to nasal swabbing, on average, across all completed biweekly study visits. c Odds ratio effect measures were estimated using logistic regression models with a generalized estimating equation (GEE) and an exchangeable correlation matrix to account for the non-independence of observations within the same household. ORs were adjusted for age and sex of IHO workers. Figure S4. Temporal distribution of multidrug-resistant and livestock-associated Staphylococcus aureus nasal carriage outcomes among 79 household contacts of industrial hog operation (IHO) workers at biweekly sampling intervals over four months, stratified by reported protective face mask usage among IHO worker(s) living in the household, North Carolina, USA, 2013-2014.
Note. BL = baseline study visit sampling time point. Biweekly sampling time points indicated by study visit columns 1-8. IHO = industrial hog operation. Black boxes indicate sampling points that were positive for the outcome indicated. White boxes without text indicate sampling time points that were negative for the indicated outcome. Gray boxes indicate missing data (nasal swabs not collected or not analyzed). OR = odds ratio. CI = confidence interval. a IHO worker(s) living in the household reported wearing a face mask <80% of the time during the one week prior to nasal swabbing, on average, during up to 8 completed biweekly study visits. b IHO worker(s) living in the household reported wearing a face mask ≥80% of the time during the one week prior to nasal swabbing, on average, during up to 8 completed biweekly study visits. c Odds ratios were estimated using logistic regression models with a generalized estimating equation (GEE) and an exchangeable correlation matrix to account for the non-independence of observations within the same household. ORs were adjusted for the age and sex of household members. Figure S5. Average log-transformed Staphylococcus aureus colony forming units (CFU) among intermittent and persistent nasal carriers of S. aureus, and S. aureus putatively associated with CC398 or CC9, 2013-2014.
Note. CFU=Colony forming units. IHO=Industrial hog operation. Individuals with >0% and <80% of swabs positive for an outcome were intermittent carriers. Individuals with ≥80% of swabs positive for an outcome were persistent carriers. We assumed all colonies with S. aureus morphology that grew on CHROMagar Staph aureus were truly S. aureus for these calculations. Prior to log transformation, we imputed a value of five CFUs for nasal swabs that were S. aureuspositive only after enrichment and a value of one CFU as the lower limit of detection for swabs that remained S. aureusnegative after enrichment. Points represent mean log 10 S. aureus CFU among swabs that were positive for the stated outcome by culture. Vertical lines indicate 95% confidence intervals for each mean. n=number of swabs contributing to the calculation.