Agricultural and Biosystems EngineeringPublications Agricultural and Biosystems Engineering

2015

The Efficiency of Biofilters at Mitigating AirborneMRSA from a Swine NurseryDwight D. FergusonUniversity of Iowa

Tara C. SmithUniversity of Iowa

Kelley J. DonhamUniversity of Iowa

Steven J. HoffIowa State University, hoffer@iastate.edu

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Journal of Agricultural Safety and Health 21(4): 217-227 © 2015 ASABE ISSN 1074-7583 DOI 10.13031/jash.21.10716 217

The Efficiency of Biofilters at Mitigating Airborne MRSA from a Swine Nursery

D. D. Ferguson, T. C. Smith, K. J. Donham, S. J. Hoff

ABSTRACT. Our prior studies have been in agreement with other researchers in detecting airborne methicillin-resistant Staphylococcus aureus (MRSA) inside and downwind of a swine housing facility. MRSA emitted in the exhaust air of swine facilities creates a poten-tial risk of transmission of these organisms to people in the general area of these facilities as well as to other animals. This study investigated a possible means of reducing those risks. We investigated the efficiency of biofilters to remove MRSA from the exhaust air of a swine building. Two types of biofilter media (hardwood chips and western red cedar shredded bark) were evaluated. Efficiency was measured by assessing both viable MRSA (viable cascade impactor) and dust particles (optical particle courter) in the pre-filtered and post-filtered air of a functioning swine production facility. Our study revealed that hardwood chips were respectively 92% and 88% efficient in removing viable MRSA and total dust particles. Western red cedar was 95% efficient in removing viable MRSA and 86% efficient in removing dust particles. Our findings suggest that biofilters can be used as effective engineering controls to mitigate the transmission of aerosolized MRSA in the exhaust air of enclosed swine housing facilities. Keywords. Airborne MRSA, Air sampling, Bioaerosol, Biofilters, Confined animal feeding operation, Swine, Zoonosis.

nimal feeding operations have been shown to be sources of air contaminants such as odors, gases, dust, endotoxins, bacteria, and antibiotic-resistant bacteria (Chien et al., 2011; Donham, 1991; Rylander et al., 1989). Workers inside animal feeding

operations are exposed to these air contaminants, which results in the risk of respiratory illnesses. Potential symptoms of health hazards associated with working in animal feeding operations include chest tightness, wheezing, coughing, and excess sputum production. Further, organic toxic dust syndrome, gastrointestinal illness, and immunologic problems have been associated with work inside swine buildings (Andersen et al., 2004; Crook et al., 1991; Donham and Thorne, 1994; Thorne, 2006). Swine workers and pigs inside confined animal feeding operations (CAFOs) have also been found to be colonized with antibiotic-resistant bacteria such as methicillin-resistant Staphylococcus aureus (MRSA) (Smith et al., 2009). Historically, MRSA was identified as a hospital-acquired infection, and it was not until the past decade that MRSA was determined to exist in the general community and in livestock facilities. Swine CAFOs have been shown to transmit air contaminants from

Submitted for review in April 2014 as manuscript number JASH 10716; approved for publication by the

Ergonomics, Safety, & Health Community of ASABE in June 2015. The authors are Dwight D. Ferguson, Graduate Student, Department of Occupational and Environmental

Health, Tara C. Smith, Associate Professor, Department of Epidemiology, and Kelley J. Donham, Professor, Department of Occupational and Environmental Health, University of Iowa, Iowa City, Iowa; Steven J. Hoff, ASABE Fellow, Professor, Department of Agricultural and Biosystems Engineering, Iowa State University, Ames, Iowa. Corresponding author: Dwight D. Ferguson, 329 CPHB, 105 River St., University of Iowa, Iowa City, IA 52242; phone: 319-325-0729; e-mail: dwight-ferguson@uiowa.edu.

A

218 Journal of Agricultural Safety and Health

their exhaust ventilation systems to nearby communities (Donham et al., 2006; Heederik et al., 2007). The emission of airborne antibiotic-resistant bacteria as well as other air con-taminants from swine CAFOs can potentially pose a public health concern (Bunton et al., 2007; Donham et al., 2006; Gibbs et al., 2006; Hamscher et al., 2003; Hoff et al., 2006; Rule et al., 2005).

Donham et al. (2006) and Gibbs et al. (2006) conducted studies which showed that air sampled in residential areas near swine CAFOs, within 4828 m (15,840 ft) and 150 m (492 ft), respectively, contained contaminants from swine CAFOs, including antibiotic-resistant bacteria (Donham et al., 2006; Green et al., 2006). People living near swine CAFOs have reported respiratory symptoms similar to those of swine workers and veterinarians (Schi-nasi et al., 2011; Wing and Wolf, 2000). Of special concern is the potential public health risk to young people in agricultural communities that include swine CAFOs. Children in schools near swine CAFOs may be exposed to airborne contaminants that may include MRSA emitted from swine CAFOs. Students in schools near swine CAFOs have higher rates of wheezing than students in schools at greater distances from swine CAFOs (Mer-chant et al., 2005; Mirabelli et al., 2006). Antibiotic-resistant S. aureus has been detected downwind of CAFOs and in residential homes, at 150 m (492 ft) and 80 m (262 ft), respec-tively (Gandara et al., 2006; Green et al., 2006). Although MRSA exposure from livestock has as-yet undefined public health and occupational health consequences, the precaution-ary principle suggests that control methods need to be investigated to mitigate the emission of MRSA and other contaminants in the exhaust air of swine CAFOs.

Biofilters, which generally use compost or wood chips to biologically degrade air pol-lutants, have been used to reduce odor emissions from swine CAFOs (Chen et al., 2009). Evaluations of biofilters have shown them to be efficient at mitigating odor emissions from swine CAFOs (Barth et al., 2002; Chen et al., 2009; Sheridan et al., 2002). Biofilters have also been shown to remove ammonia and reduce the concentration levels of dust, endotox-ins, and bacteria from CAFOs (Martens et al., 2001; Tymczyna et al., 2007).

The objective of this study was to determine the efficiency of biofilters in mitigating airborne MRSA emitted from a swine CAFO. The efficiency of biofilters in reducing the concentration of airborne MRSA particles was tested using a mobile biofilter unit. A work-ing swine facility in which the pigs, workers, and air were culture positive for MRSA was fitted with ductwork that connected an exhaust fan to the mobile biofilter unit. The duct-work allowed exhaust air from the swine feeding facility to be pulled through the biofilters, which contained two different types of media: hardwood chips (HWC) and western red cedar shredded bark (WRC).

Materials and Methods Study Site

The study site was selected as representative of modern swine production facilities. Fur-ther, we previously documented that the workers and swine at this facility were culture positive for MRSA (Smith et al., 2009). The producers were willing to cooperate with this study, informed consent was obtained, and all institutional review board (IRB) require-ments were followed. The veterinarian for the facility helped facilitate the study, providing consultation for conducting sampling at the facility. The study site consisted of two build-ings and produced approximately 48,000 feeder pigs per year. Pigs entered the buildings at 14 days of age and left at the age of 60 days, weighing approximately 23 kg (50 lb). The

21(4): 217-227 219

stocking density of the two buildings was one pig per 0.37 m2 (4 ft2). Ventilation for the facility was provided by sixteen 61 cm (24 in.) and eight 36 cm

(14 in.) wall fans (both thermostat controlled) and eight 23 cm (9 in.) continuous pit fans. The facility had curtains on both sidewalls for increased ventilation during warm seasons. The volume of the study room was 364 m3 (12,847 ft3). The sampled facility was power washed with detergent and disinfectant (Keno X5, CID Lines, Ypres, Belgium) between cycling of hogs (46 days) due to the all-in, all-out management at the site. The active in-gredients of the disinfectant were hydrogen peroxide and peroxyacetic acid. The topogra-phy of the area surrounding the facility was flat with no wind buffers.

Biofilter Unit We used a modified version of a mobile biofilter design in collaboration with the Air

Dispersion Laboratory (under the direction of Dr. Steven Hoff) at Iowa State University (Chen et al., 2008). The modified biofilter design was tested and refined at the Air Disper-sion Laboratory before field testing was performed to verify that constant airflow (1400 L min-1) and pressure drop (16 ±1 Pa for HWC; 27 ±1 Pa for WRC) were maintained. For the field test, a six-stage sampler (N-6 ACI, Andersen Samplers, Inc., Atlanta, Ga.) and an optical particle counter (OPC) (Grimm Technologies, Inc., Douglasville, Ga.) were used to assess the particulate matter and viable MRSA content of the air inside the building, in the filtered air, and from a negative control that contained no filter media (Cheng, 2008; Lundholm, 1982; Predicala et al., 2002).

A plenum (duct) was connected from an exhaust fan of the CAFO to the biofilters. The mobile biofilter unit was composed of eight 190 L (50 gal) barrels that contained one of two biofilter media (fig. 1): HWC of 5 cm length or WRC shredded bark (Chen et al., 2009). Three barrels contained HWC, three barrels contained WRC, two barrels were neg-ative controls. The media depth was 25 cm for both media treatments. Media moisture content was in the range of 50% to 60% (wet basis). Media moisture was measured with sensors (ECH2O EC-20, Decagon Devices, Inc., Pullman, Wash.), and water was added to the tops of the barrels using an automatic spray nozzle.

Prior to biofilter use, media chips were evaluated for MRSA in the laboratory. We mod-ified the method of O’Brien et al. (2012) by using media chips instead of meat. Briefly, 10 g of media chips were placed in 100 mL of staph enrichment broth and incubated overnight at 35°C. The broth was then plated onto CHROMagar and CNA plates using the spread plate technique and incubated for another 24 to 48 h. The plates were found to be negative.

We assessed the air inside the CAFO for the presence of viable MRSA in comparison to the exhaust air. The exhaust air from the CAFO was assessed for viable MRSA to com-pare the efficiency of the two different media (HWC and WRC). The empty bed retention time of the air within the biofilters was adjusted to 4 s as determined by Chen et al. (2009). An N-6 ACI sampler (using only three stages for collection) was used to sample air at three locations: the center of the CAFO in an empty pen, the exhaust of the biofilters (fig. 2), and the negative control. Stage one of the N-6 ACI sampler collected MRSA particulate matter in the size range of 7 μm and larger, stage two collected MRSA particulate matter in the size range of 4.7 to 7 μm, and stage five collected MRSA particulate matter in the size range of 1.1 to 2.1 μm.

220 Journal of Agricultural Safety and Health

Air sampling times of 30 s and 1 min were used inside the CAFO. Sampling times for the biofiltered air and the negative control were 15 and 20 min, respectively. The sampling times were selected based on preliminary trials. During the preliminary trials, sampling for more than 1 min inside the CAFO resulted in particles too numerous to count, and sampling for less than 30 s was insufficient. Preliminary trials using a filter showed that sampling for less than 15 min was insufficient to collect samples, and sampling for more than 20 min led to desiccation of the particulate matter. Environmental conditions inside the CAFO and atmospheric conditions outside the CAFO, including temperature, relative humidity, and CO and CO2 concentrations, were measured (Cheng, 2008; Edimansyah et al., 2009; Mid-dendorf et al., 2001). Sampling was performed during four days in January. Each trial was conducted in triplicate for data reliability.

Air was sampled using CHROMagar plates as the collection media for N-6 ACI stages one, two, and five. After each sampling period, the culture plates were sealed with tape, labeled, placed in Ziploc bags, and finally placed (upside down) in a cooler with ice packs for transport to the laboratory. Bacteria concentration (CFU m-3) was determined by the number of colony-forming units (CFU) per plate divided by the product of sampling time and volume of air collected.

Removal efficiency of the biofilters was defined as the difference between the concen-tration of MRSA colony-forming units and particulate matter counts of the negative control air inside the building and the concentration of the same contaminants in the air that

Figure 1. Mobile biofilter unit.

Mobile biofilter unit

Plenum connected to exhaust fan Barrels with biofilter media

21(4): 217-227 221

Figure 2. Sampling air through biofilter media.

passed through the biofilters, divided by the unfiltered particulate matter. The removal ef-ficiency is reported as a percentage:

Removal efficiency (%) =

(Negative control particulate matter − Filtered particulate matter)

÷ Negative control particulate matter × 100

Bacterial Diagnostics In the laboratory, the CHROMagar MRSA plates were incubated at 35°C for 48 h. Rep-

resentative colonies from the CHROMagar plates were subcultured on Columbia CNA (Remel, Lenexa, Kans.) for diagnostic testing. Identification tests for S. aureus isolates included the catalase test, the coagulase test, and the S. aureus latex agglutination assay (Pastorex Staph-plus, Bio-Rad Laboratories, Inc., Hercules, Cal.). Methicillin resistance was confirmed by testing for the presence of penicillin binding protein (PBP2′) (MRSA latex agglutination test, Oxoid, Ltd., Basingstoke, U.K.). Positive and negative controls were used for all tests.

Statistics Statistical analyses, including paired two-sample mean t-tests, were used to compare the

efficiency of the two types of media at removing total dust particulate matter. Significance was determined at p ≤ 0.05.

222 Journal of Agricultural Safety and Health

Results Table 1 shows a comparison of the mean concentration of total dust particulate matter

inside the building to the mean concentrations for the negative control, HWC biofilter, and WRC biofilter. Significant differences were found between the mean concentration of total dust particulate matter inside the building and the mean concentrations for both HWC and WRC. No significant difference was found between the mean concentrations inside the building and for the negative control.

Figure 3 shows the OPC results for non-viable particles for the HWC biofilter. The OPC measured the size of dust particulate matter through 15 channels with size ranges from 0.4 μm to >20 μm. The HWC biofilter was 89% efficient in removing dust particulate matter with a mean particle size of 1.8 μm, 88% efficient with a mean particle size of 4.5 μm, and 97% efficient with a mean particle size above 10 μm.

The removal efficiencies of the WRC biofilter for non-viable particulate matter using the OPC are shown with standard error bars in figure 4. The WRC biofilter was 83% effi-cient in removing dust particulate matter with a mean particle size of 0.9 μm, 59% efficient with a mean particle size of 1.8 μm, and 86% efficient with a mean particle size of greater than 8.75 μm.

Results for the removal efficiency of the HWC biofilter for viable MRSA particulate matter as determined by the N-6 ACI sampler are shown in table 2. The results show that the HWC biofilter was 92% efficient in removing viable MRSA particulate matter with a mean particle size of 5.85 μm. The removal efficiency of the WRC biofilter for viable MRSA particulate matter (table 3) shows that the WRC biofilter was 100% efficient in removing viable MRSA particulate matter with a mean particle size of 5.85 μm.

Table 1. Paired t-test comparison with total dust particulate matter inside the swine facility. Location Mean Concentration (average counts L-1) p-Value

Negative control 11,770.59 0.14 HWC biofilter 3,872.30 0.01 WRC biofilter 1,745.22 0.02

Figure 3. Dust particulate matter removal efficiency of HWC biofilter as determined by OPC.

0

20

40

60

80

100

120

-5 0 5 10 15 20 25 30

Effic

ienc

y (%

)

Particle Diameter (μm)

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Figure 4. Dust particulate matter removal efficiency of WRC biofilter as determined by OPC.

Table 2. MRSA removal efficiency of HWC biofilter as determined by N-6 ACI sampler.

Particle Diameter (μm) Negative Control (CFU m-3)

Filtered Air (CFU m-3)

Efficiency (%) Lower Limit Upper Limit Average

1.1 2.1 1.60 3.53 0.79 77.78 4.7 7 5.85 5.10 0.39 92.31 7 - 20.00 2.75 0 100

Table 3. MRSA removal efficiency of WRC biofilter as determined by N-6 ACI sampler.

Particle Diameter (μm) Negative Control (CFU m-3)

Filtered Air (CFU m-3)

Efficiency (%) Lower Limit Upper Limit Average

1.1 2.1 1.60 3.53 0.39 88.95 4.7 7 5.85 5.10 0 100 7 - 20.00 2.75 0 100

Discussion Our results showed that HWC and WRC were highly efficient biofilter media for miti-

gating emissions of viable MRSA particulate matter in the exhaust air from a swine feeding facility. The HWC biofilter had removal efficiency of 77% for particulate matter with a mean particle size of 1.6 μm. The removal efficiency of the HWC biofilter increased as the bioaerosol particle size increased. WRC was highly effective for removing particulate mat-ter with mean diameters of 1.6 to 5.85 μm. We speculate that the difference in removal efficiencies shown by the two biofilter media may have been due to the coarseness of the media, which may have affected the biofilter porosity (Nicolai and Janni, 2001). The HWC (>5 cm) media were coarser than the WRC (

224 Journal of Agricultural Safety and Health

of the HWC media. On the other hand, the WRC media were shredded pieces that inter-twined closely, thus making the WRC biofilter less porous than the HWC biofilter. Because the WRC media were less porous than the HWC media, the WRC biofilter had higher removal efficiencies for smaller-size particulate matter compared to the HWC biofilter. We postulate that the difference in removal efficiencies may have been due to the biofilter media used (Chen et al., 2009). Nevertheless, the results showed that HWC and WRC were both highly efficient biofilter media for mitigating emissions of MRSA from a swine feed-ing facility.

Although this is the first study of the effectiveness of biofilters for mitigating emissions of MRSA, other studies have reported the effectiveness of biofilters for removing other contaminants. Tymczyna et al. (2007) found that biofilter media were efficient at retaining dust, gram-negative bacteria, and endotoxins emitted from a chicken hatchery. Martens et al. (2001) found that biofilters were efficient at removing bioaerosols from pig facilities. In addition to being the first study of biofilter effectiveness for MRSA mitigation, this study has advanced the field by evaluating the removal efficiencies of different media (HWC and WRC). Both HWC and WRC were efficient at mitigating emissions of total dust particles. WRC was more efficient at mitigation of airborne viable MRSA. Prior re-search (Barth et al., 2002; Martens et al., 2001; Tymczyna et al., 2007), along with the results of our study, indicated that biofilters can be efficient at reducing emissions of air-borne MRSA, gram-negative bacteria, endotoxins, and various gases in the exhaust venti-lation systems of swine feeding facilities.

Our study had several strengths. This is the first study that we are aware of to evaluate the efficiency of biofilters in reducing the emission of airborne MRSA from a swine facil-ity. We also conducted simultaneous assessment of real-time dust concentrations and via-ble particulate matter. Previous research showed that bacteria in swine CAFOs travel by attaching to particulates in the bioaerosol airstream (Donham et al., 1986). The results of the total and viable particulate matter assessment revealed a correlation between total and viable particle concentrations. This finding is important for control implications, suggest-ing that dust control will also affect MRSA aerosol exposures.

There were also limitations in this study. The one-month study duration prevented more extensive sampling from being conducted. The all-in, all-out management of the swine facility prevented a longer study period. The small sample size precludes generalization to different types of buildings and different geographical and climatic regions.

Despite the limitations of our study, we believe that there are important findings relative to community and public health. Green et al. (2006) found that antibiotic-resistant bacteria were emitted by the exhaust ventilation systems of swine feeding facilities at concentra-tions that can cause potential health problems for people and animals living within 150 m of the facility. Of special concern, S. aureus was the most recovered species downwind of a swine facility in a study conducted by Gibbs et al. (2006). Gandara et al. (2006) found that antibiotic-resistant S. aureus was detected in residential homes, although the source was not identified. The results of our studies suggest that airborne viable MRSA particles can be emitted by the exhaust ventilation systems of animal feeding facilities and can po-tentially travel in the airstream to nearby outdoor worksites, rural residences, and commu-nities.

Our results showed that biofilters can be efficiently used to reduce the emission of viable MRSA particles from swine facilities to mitigate transmission of this antibiotic-resistant pathogen as well as total dust particulate matter.

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Conclusion Our results showed that HWC and WRC were highly efficient as biofilter media for

mitigating emissions of airborne viable MRSA particulate matter from a swine facility that tested positive for MRSA in pigs and swine workers. We previously showed that MRSA can be detected at 215 m (705 ft) from a swine CAFO, which is farther than the downwind emission detection by Green et al. (2006). Our current findings showed that biofilters can be used to mitigate airborne transmission of MRSA particles from an MRSA-positive swine facility. Biofilters have previously been shown to be effective at reducing emissions of odors and gases from swine facilities. Our results suggest that biofilters can also be used to reduce emissions of viable MRSA particles from swine facilities. This finding suggests that biofilters can assist in reducing the risk of MRSA transmission to people and animals near swine buildings and assist in reducing the risk of transmission of this antibiotic-re-sistant pathogen between buildings on multi-building farms. We recommend that future studies be done to determine if these results can be duplicated. We also suggest further studies to determine if MRSA can be detected beyond the current regulated separation dis-tances for CAFOs from surrounding communities. These future studies can help determine if the current separation distances for CAFOs are adequate or if the separation distances need to be re-evaluated. Furthermore, future studies are needed to determine the necessary distance between swine buildings on the same farm to prevent MRSA transmission through the air between buildings.

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2015The Efficiency of Biofilters at Mitigating Airborne MRSA from a Swine NurseryDwight D. FergusonTara C. SmithKelley J. DonhamSteven J. Hoff

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