Joan A. Casey

High-Density Livestock Operations, Crop Field Application of Manure, and Risk of Community-Associated Methicillin-Resistant Staphylococcus aureus Infection in Pennsylvania

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.

Unconventional natural gas development and birth outcomes in Pennsylvania, USA

Background: Unconventional natural gas development has expanded rapidly. In Pennsylvania, the number of producing wells increased from 0 in 2005 to 3,689 in 2013. Few publications have focused on unconventional natural gas development and birth outcomes. Methods: We performed a retrospective cohort study using electronic health record data on 9,384 mothers linked to 10,946 neonates in the Geisinger Health System from January 2009 to January 2013. We estimated cumulative exposure to unconventional natural gas development activity with an inverse-distance squared model that incorporated distance to the mother’s home; dates and durations of well pad development, drilling, and hydraulic fracturing; and production volume during the pregnancy. We used multilevel linear and logistic regression models to examine associations between activity index quartile and term birth weight, preterm birth, low 5-minute Apgar score and small size for gestational age birth, while controlling for potential confounding variables. Results: In adjusted models, there was an association between unconventional natural gas development activity and preterm birth that increased across quartiles, with a fourth quartile odds ratio of 1.4 (95% confidence interval = 1.0, 1.9). There were no associations of activity with Apgar score, small for gestational age birth, or term birth weight (after adjustment for year). In a posthoc analysis, there was an association with physician-recorded high-risk pregnancy identified from the problem list (fourth vs. first quartile, 1.3 [95% confidence interval = 1.1, 1.7]). Conclusion: Prenatal residential exposure to unconventional natural gas development activity was associated with two pregnancy outcomes, adding to evidence that unconventional natural gas development may impact health. See Video Abstract at http://links.lww.com/EDE/B14.

A population-based study of the epidemiology and clinical features of methicillin-resistant Staphylococcus aureus infection in Pennsylvania, 2001-2010.

No U.S. general population-based study has characterized the epidemiology and risk factors, including skin and soft tissue infection (SSTI), for healthcare-associated (HA) and community-associated (CA) methicillin-resistant Staphylococcus aureus (MRSA). We estimated the incidence of HA- and CA-MRSA and SSTI over a 9-year period using electronic health record data from the Geisinger Clinic in Pennsylvania. MRSA cases were frequency-matched to SSTI cases and controls in a nested case-control analysis. Logistic regression was used to assess risk factors, while accounting for antibiotic administration. We identified 1713 incident CA- and 1506 HA-MRSA cases and 78 216 SSTI cases. On average, from 2005 to 2009, the annual incidence of CA-MRSA increased by 34%, HA-MRSA by 7%, and SSTI by 4%. Age, season, community socioeconomic deprivation, obesity, smoking, previous SSTI, and antibiotic administration were identified as independent risk factors for CA-MRSA.

Greenness and Birth Outcomes in a Range of Pennsylvania Communities

Living in communities with more vegetation during pregnancy has been associated with higher birth weights, but fewer studies have evaluated other birth outcomes, and only one has been conducted in the Eastern United States, in regions with a broad range, including high levels, of greenness. We evaluated associations between prenatal residential greenness and birth outcomes (term birth weight, small for gestational age, preterm birth, and low 5 min Apgar score) across a range of community types using electronic health record data from 2006–2013 from the Geisinger Health System in Pennsylvania. We assigned greenness based on mother’s geocoded address using the normalized difference vegetation index from satellite imagery. We used propensity scores to restrict the study population to comparable groups among those living in green vs. less-green areas. Analyses were adjusted for demographic, clinical, and environmental covariates, and stratified by community type (city, borough, and township). In cities, higher greenness (tertiles 2–3 vs. 1) was protective for both preterm (OR = 0.78, 95% CI: 0.61–0.99) and small for gestational age birth (OR = 0.73, 95% CI: 0.58–0.97), but not birth weight or Apgar score. We did not observe associations between greenness and birth outcomes in adjusted models in boroughs or townships. These results add to the evidence that greener cities might be healthier cities.

High-density livestock production and molecularly characterized MRSA infections in Pennsylvania.

Background: European studies suggest that living near high-density livestock production increases the risk of sequence type (ST) 398 methicillin-resistant Staphylococcus aureus (MRSA) colonization. To our knowledge, no studies have evaluated associations between livestock production and human infection by other strain types. Objectives: We evaluated associations between MRSA molecular subgroups and high-density livestock production. Methods: 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 (PVL) and scn genes. We compared patients with one of two specific MRSA strains with 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). Results: 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 vs. 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). Conclusions: Our findings suggest that other MRSA strains, beyond ST398, may be involved in livestock-associated MRSA infection in the United States. Citation: Casey JA, Shopsin B, Cosgrove SE, Nachman KE, Curriero FC, Rose HR, Schwartz BS. 2014. High-density livestock production and molecularly characterized MRSA infections in Pennsylvania. Environ Health Perspect 122:464–470; http://dx.doi.org/10.1289/ehp.1307370

Predictors of Indoor Radon Concentrations in Pennsylvania, 1989–2013

Background Radon is the second-leading cause of lung cancer worldwide. Most indoor exposure occurs by diffusion of soil gas. Radon is also found in well water, natural gas, and ambient air. Pennsylvania has high indoor radon concentrations; buildings are often tested during real estate transactions, with results reported to the Department of Environmental Protection (PADEP). Objectives We evaluated predictors of indoor radon concentrations. Methods Using first-floor and basement indoor radon results reported to the PADEP between 1987 and 2013, we evaluated associations of radon concentrations (natural log transformed) with geology, water source, building characteristics, season, weather, community socioeconomic status, community type, and unconventional natural gas development measures based on drilled and producing wells. Results Primary analysis included 866,735 first measurements by building, with the large majority from homes. The geologic rock layer on which the building sat was strongly associated with radon concentration (e.g., Axemann Formation, median = 365 Bq/m3, IQR = 167–679 vs. Stockton Formation, median = 93 Bq/m3, IQR = 52–178). In adjusted analysis, buildings using well water had 21% higher concentrations (β = 0.191, 95% CI: 0.184, 0.198). Buildings in cities (vs. townships) had lower concentrations (β = –0.323, 95% CI: –0.333, –0.314). When we included multiple tests per building, concentrations declined with repeated measurements over time. Between 2005 and 2013, 7,469 unconventional wells were drilled in Pennsylvania. Basement radon concentrations fluctuated between 1987 and 2003, but began an upward trend from 2004 to 2012 in all county categories (p < 0.001), with higher levels in counties having ≥ 100 drilled wells versus counties with none, and with highest levels in the Reading Prong. Conclusions Geologic unit, well water, community, weather, and unconventional natural gas development were associated with indoor radon concentrations. Future studies should include direct environmental measurement of radon, as well as building features unavailable for this analysis. Citation Casey JA, Ogburn EL, Rasmussen SG, Irving JK, Pollak J, Locke PA, Schwartz BS. 2015. Predictors of indoor radon concentrations in Pennsylvania, 1989–2013. Environ Health Perspect 123:1130–1137; http://dx.doi.org/10.1289/ehp.1409014

Measures of SES for Electronic Health Record-based Research

INTRODUCTION Although infrequently recorded in electronic health records (EHRs), measures of SES are essential to describe health inequalities and account for confounding in epidemiologic research. Medical Assistance (i.e., Medicaid) is often used as a surrogate for SES, but correspondence between conventional SES and Medical Assistance has been insufficiently studied. METHODS Geisinger Clinic EHR data from 2001 to 2014 and a 2014 questionnaire were used to create six SES measures: EHR-derived Medical Assistance and proportion of time under observation on Medical Assistance; educational attainment, income, and marital status; and area-level poverty. Analyzed in 2016-2017, associations of SES measures with obesity, hypertension, type 2 diabetes, chronic rhinosinusitis, fatigue, and migraine headache were assessed using weighted age- and sex-adjusted logistic regression. RESULTS Among 5,550 participants (interquartile range, 39.6-57.5 years, 65.9% female), 83% never used Medical Assistance. All SES measures were correlated (Spearmans p≤0.4). Medical Assistance was significantly associated with all six health outcomes in adjusted models. For example, the OR for prevalent type 2 diabetes associated with Medical Assistance was 1.7 (95% CI=1.3, 2.2); the OR for high school versus college graduates was 1.7 (95% CI=1.2, 2.5). Medical Assistance was an imperfect proxy for SES: associations between conventional SES measures and health were attenuated <20% after adjustment for Medical Assistance. CONCLUSIONS Because systematically collected SES measures are rarely available in EHRs and are unlikely to appear soon, researchers can use EHR-based Medical Assistance to describe inequalities. As SES has many domains, researchers who use Medical Assistance to evaluate the association of SES with health should expect substantial unmeasured confounding.

Proximity to Industrial Food Animal Production and Asthma Exacerbations in Pennsylvania, 2005–2012

The research on industrial food animal production (IFAP) and asthma exacerbations in the United States has relied on small sample sizes and/or self-reported outcomes. We assessed associations of proximity to large-scale and densely stocked swine and dairy/veal IFAP with three types of asthma exacerbations: hospitalizations, emergency encounters, and oral corticosteroid (OCS) medication orders from Geisinger Clinic in Pennsylvania. We used a diagnosis code (International Classification of Diseases, 9th Revision, Clinical Modification code 493.x) and medication orders from electronic health records to identify these exacerbations among asthma patients (n = 35,269) from 2005–2012. We compared residential proximity to swine or dairy/veal IFAP (dichotomized as <3 miles (4.8 km) or ≥3 miles) among asthma patients with and without exacerbations and estimated odds ratios using multilevel logistic regression. In adjusted models, proximity to IFAP was associated (odds ratio (95% confidence interval)) with OCS orders (1.11 (1.04–1.19)) and hospitalizations (1.29 (1.15–1.46)), but not emergency encounters (1.12 (0.91–1.37)). This study contributes to growing evidence that IFAP may impact health, in this case clinically-documented asthma exacerbations. No prior study has evaluated the association of IFAP and clinically-documented asthma exacerbations in the United States.

Race, Ethnicity, Income Concentration and 10-Year Change in Urban Greenness in the United States

Background: Cross-sectional studies suggest urban greenness is unequally distributed by neighborhood demographics. However, the extent to which inequalities in greenness have changed over time remains unknown. Methods: We estimated 2001 and 2011 greenness using Moderate-resolution Imaging Spectroradiometer (MODIS) satellite-derived normalized difference vegetative index (NDVI) in 59,483 urban census tracts in the contiguous U.S. We fit spatial error models to estimate the association between baseline census tract demographic composition in 2000 and (1) 2001 greenness and (2) change in greenness between 2001 and 2011. Results: In models adjusted for population density, climatic factors, housing tenure, and Index of Concentration at the Extremes for income (ICE), an SD increase in percent White residents (a 30% increase) in 2000 was associated with 0.021 (95% CI: 0.018, 0.023) higher 2001 NDVI. We observed a stepwise reduction in 2001 NDVI with increased concentration of poverty. Tracts with a higher proportion of Hispanic residents in 2000 lost a small, statistically significant amount of greenness between 2001 and 2011 while tracts with higher proportions of Whites experienced a small, statistically significant increase in greenness over the same period. Conclusions: Census tracts with a higher proportion of racial/ethnic minorities, compared to a higher proportion of White residents, had less greenness in 2001 and lost more greenness between 2001 and 2011. Policies are needed to increase greenness, a health-promoting neighborhood asset, in disadvantaged communities.

Separating the Bruce and Trivers‐Willard effects in theory and in human data

Theories of reproductive suppression predict that natural selection would conserve mechanisms that abort the gestation of offspring otherwise unlikely to thrive in prevailing environments. Research reports evidence among humans of at least two such mechanisms—the Trivers‐Willard and Bruce Effects. No literature, however, compares the mechanisms nor estimates their relative contribution to observed characteristics of human birth cohorts. We describe similarities and differences between the Trivers‐Willard and Bruce Effects and explore high quality historical data from Sweden to determine which mechanism better describes temporal variation in the ratio of males to females in birth cohorts.