High-Density Livestock Operations, Crop Field Application of Manure, and Risk of Community-Associated MRSA Infection in Pennsylvania

Department of Environmental Health Sciences, Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland2Johns Hopkins School of Medicine, Baltimore, Maryland.
JAMA Internal Medicine (Impact Factor: 13.12). 09/2013; 173(21). DOI: 10.1001/jamainternmed.2013.10408
Source: PubMed


IMPORTANCE Nearly 80% of antibiotics in the United States are sold for use in livestock feeds. The manure produced by these animals contains antibiotic-resistant bacteria, resistance genes, and antibiotics and is subsequently applied to crop fields, where it may put community members at risk for antibiotic-resistant infections. OBJECTIVE To assess the association between individual exposure to swine and dairy/veal industrial agriculture and risk of methicillin-resistant Staphylococcus aureus (MRSA) infection. DESIGN, SETTING, AND PARTICIPANTS A population-based, nested case-control study of primary care patients from a single health care system in Pennsylvania from 2005 to 2010. Incident MRSA cases were identified using electronic health records, classified as community-associated MRSA or health care-associated MRSA, and frequency matched to randomly selected controls and patients with skin and soft-tissue infection. Nutrient management plans were used to create 2 exposure variables: seasonal crop field manure application and number of livestock animals at the operation. In a substudy, we collected 200 isolates from patients stratified by location of diagnosis and proximity to livestock operations. MAIN OUTCOMES AND MEASURES Community-associated MRSA, health care-associated MRSA, and skin and soft-tissue infection status (with no history of MRSA) compared with controls. RESULTS From a total population of 446 480 patients, 1539 community-associated MRSA, 1335 health care-associated MRSA, 2895 skin and soft-tissue infection cases, and 2914 controls were included. After adjustment for MRSA risk factors, the highest quartile of swine crop field exposure was significantly associated with community-associated MRSA, health care-associated MRSA, and skin and soft-tissue infection case status (adjusted odds ratios, 1.38 [95% CI, 1.13-1.69], 1.30 [95% CI, 1.05-1.61], and 1.37 [95% CI, 1.18-1.60], respectively); and there was a trend of increasing odds across quartiles for each outcome (P ≤ .01 for trend in all comparisons). There were similar but weaker associations of swine operations with community-associated MRSA and skin and soft-tissue infection. Molecular testing of 200 isolates identified 31 unique spa types, none of which corresponded to CC398 (clonal complex 398), but some have been previously found in swine. CONCLUSIONS AND RELEVANCE Proximity to swine manure application to crop fields and livestock operations each was associated with MRSA and skin and soft-tissue infection. These findings contribute to the growing concern about the potential public health impacts of high-density livestock production.

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Available from: Joan A. Casey, Nov 17, 2014
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    • "Because of this, and because none of the participants of this study had recent direct contact with livestock, it is not surprising that all of the isolates were scn positive and that MRSA CC398 [38,39] was not present. Similar to our findings, in a study in Pennsylvania, MRSA CC398 was not detected among patients with MRSA infections; however, MRSA infection cases were positively associated with indicators of environmental swine exposures [37]. "
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    ABSTRACT: Background Distinct strains of methicillin resistant Staphylococcus aureus (MRSA) have been identified on livestock and livestock workers. Industrial food animal production may be an important environmental reservoir for human carriage of these pathogenic bacteria. The objective of this study was to investigate environmental and occupational exposures associated with nasal carriage of MRSA in patients hospitalized at Vidant Medical Center, a tertiary hospital serving a region with intensive livestock production in eastern North Carolina. Methods MRSA nasal carriage was identified via nasal swabs collected within 24 hours of hospital admission. MRSA carriers (cases) were gender and age matched to non-carriers (controls). Participants were interviewed about recent environmental and occupational exposures. Home addresses were geocoded and publicly available data were used to estimate the density of swine in residential census block groups of residence. Conditional logistic regression models were used to derive odds ratio (OR) estimates and 95% confidence intervals (CI). Presence of the scn gene in MRSA isolates was assessed. In addition, multi locus sequence typing (MLST) of the MRSA isolates was performed, and the Diversilab® system was used to match the isolates to USA pulsed field gel electrophoresis types. Results From July - December 2011, 117 cases and 119 controls were enrolled. A higher proportion of controls than cases were current workforce members (41.2% vs. 31.6%) Cases had a higher odds of living in census block groups with medium densities of swine (OR: 4.76, 95% CI: 1.36-16.69) and of reporting the ability to smell odor from a farm with animals when they were home (OR: 1.51, 95% CI: 0.80-2.86). Of 49 culture positive MRSA isolates, all were scn positive. Twenty-two isolates belonged to clonal complex 5. Conclusions Absence of livestock workers in this study precluded evaluation of occupational exposures. Higher odds of MRSA in medium swine density areas could reflect environmental exposure to swine or poultry.
    Full-text · Article · Jun 2014 · Environmental Health
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    • "Public access to information regarding hazardous airborne releases from IFAP operations is hindered due to exemptions in federal laws that require disclosure of such releases [15], despite research linking chronic exposure to odors from IFAP to headaches, nausea, upset stomach, mood disorders, high blood pressure, and sleep problems [16]–[20]. Additionally, there is growing evidence that livestock can transmit methicillin-resistant Staphylococcus aureus (MRSA) to humans [21]–[23]. Rural water supplies are also at risk, as IFAP-generated animal waste contaminants, including nitrates, pathogens, pharmaceuticals, metals, and hormones, can leach into ground water [24], [25]. All of these concerns may be compounded by the fact that IFAP operations are disproportionately located in low-income communities with high-percentages of minority populations [26]–[28], which are more likely to experience limited political power [29] and barriers to healthcare access [30]. "
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    ABSTRACT: Industrial food animal production (IFAP) operations adversely impact environmental public health through air, water, and soil contamination. We sought to determine how state permitting and agriculture agencies respond to these public health concerns. We conducted semi-structured qualitative interviews with staff at 12 state agencies in seven states, which were chosen based on high numbers or rapid increase of IFAP operations. The interviews served to gather information regarding agency involvement in regulating IFAP operations, the frequency and type of contacts received about public health concerns, how the agency responds to such contacts, and barriers to additional involvement. Permitting and agriculture agencies' responses to health-based IFAP concerns are constrained by significant barriers including narrow regulations, a lack of public health expertise within the agencies, and limited resources. State agencies with jurisdiction over IFAP operations are unable to adequately address relevant public health concerns due to multiple factors. Combining these results with previously published findings on barriers facing local and state health departments in the same states reveals significant gaps between these agencies regarding public health and IFAP. There is a clear need for regulations to protect public health and for public health professionals to provide complementary expertise to agencies responsible for regulating IFAP operations.
    Full-text · Article · Feb 2014 · PLoS ONE
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    • "For CO-PVL-negative MRSA, we also estimated associations with individual quartiles of exposure relative to the lowest quartile, but numbers of observations were too small to run comparable models for scn-negative MRSA. Similarly, adjustment for confounders selected based on a priori information (Casey et al. 2013a, 2013b) was limited to models of CO-PVL-negative MRSA. Specifically, we adjusted for sex, age (continuous), ever-smoking status, season of infection [winter (December–February) vs. all other seasons combined], physician order for an antibiotic in the 365 to 14 days preceding diagnosis, and ever-receiving Medical Assistance as health insurance [as a surrogate for low individual socioeconomic status (Bratu et al. 2006; Casey et al. 2013b)]. "
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    ABSTRACT: European studies suggest that living near high-density livestock production increases the risk of sequence type ST398 methicillin-resistant Staphylococcus aureus (MRSA) colonization. To our knowledge, no studies have evaluated associations between livestock production and human infection by other strain types. We evaluated associations between MRSA molecular subgroups and high-density livestock production. We conducted a yearlong 2012 prospective study on a stratified random sample of patients with culture-confirmed MRSA infection; we oversampled patients from the Geisinger Health System with exposure to high-density livestock production in Pennsylvania. Isolates were characterized using S. aureus protein A (spa) typing and detection of Panton-Valentine leukocidin and scn genes. Patients with one of two specific MRSA strains were compared to patients with all other strains of MRSA isolates using logistic regression that accounted for the sampling design, for two different exposure models: one based on the location of the animals (livestock model) and the other on crop field application of manure (crop field model). Of 196 MRSA isolates, we identified 30 spa types, 47 PVL-negative and 15 scn-negative isolates, and no ST398 MRSA. Compared with quartiles 1-3 combined, the highest quartiles of swine livestock and dairy/veal crop field exposures were positively associated with community-onset-PVL-negative MRSA (CO-PVL-negative MRSA versus all other MRSA), with adjusted odds ratios of 4.24 (95% CI: 1.60, 11.25) and 4.88 (95% CI: 1.40, 17.00), respectively. The association with CO-PVL-negative MRSA infection increased across quartiles of dairy/veal livestock exposure (trend p = 0.05). The findings suggest that other MRSA strains, beyond ST398, may be involved in livestock-associated MRSA infection in the U.S.
    Full-text · Article · Feb 2014 · Environmental Health Perspectives
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