Blake M. Hanson

Prevalence of Staphylococcus aureus and methicillin-resistant Staphylococcus aureus (MRSA) on retail meat in Iowa

Several recent studies have indicated a high prevalence of methicillin-resistant Staphylococcus aureus (MRSA) in retail-available meat. However, few studies have investigated MRSA in meat in the United States. The aim of this study was to determine the presence of Staphylococcus aureus (S. aureus) on meat samples available at retail stores. Samples of fresh raw pork, chicken, beef, and turkey were purchased from 22 food stores throughout Iowa. S. aureus strains were isolated from 27 of 165 samples, giving an overall prevalence of 16.4%. Turkey, pork, chicken, and beef had individual S. aureus prevalence rates of 19.4%, 18.2%, 17.8%, and 6.9%, respectively. Two isolates of MRSA were isolated from pork, giving an overall prevalence of 1.2%. One MRSA isolate was positive for the PVL gene. Common spa types included t034, t337, t008, and t002. These results suggest that MRSA is present on low numbers of retail meat in Iowa.

Isolation and Characterization of Methicillin-Resistant Staphylococcus aureus from Pork Farms and Visiting Veterinary Students

In the last decade livestock-associated methicillin-resistant S. aureus (LA-MRSA) has become a public health concern in many parts of the world. Sequence type 398 (ST398) has been the most commonly reported type of LA-MRSA. While many studies have focused on long-term exposure experienced by swine workers, this study focuses on short-term exposures experienced by veterinary students conducting diagnostic investigations. The objectives were to assess the rate of MRSA acquisition and longevity of carriage in students exposed to pork farms and characterize the recovered MRSA isolates. Student nasal swabs were collected immediately before and after farm visits. Pig nasal swabs and environmental sponge samples were also collected. MRSA isolates were identified biochemically and molecularly including spa typing and antimicrobial susceptibility testing. Thirty (30) veterinary students were enrolled and 40 pork farms were visited. MRSA was detected in 30% of the pork farms and in 22% of the students following an exposure to a MRSA-positive pork farm. All students found to be MRSA-positive initially following farm visit were negative for MRSA within 24 hours post visit. Most common spa types recovered were t002 (79%), t034 (16%) and t548 (4%). Spa types found in pork farms closely matched those recovered from students with few exceptions. Resistance levels to antimicrobials varied, but resistance was most commonly seen for spectinomycin, tetracyclines and neomycin. Non-ST398 MRSA isolates were more likely to be resistant to florfenicol and neomycin as well as more likely to be multidrug resistant compared to ST398 MRSA isolates. These findings indicate that MRSA can be recovered from persons visiting contaminated farms. However, the duration of carriage was very brief and most likely represents contamination of nasal passages rather than biological colonization. The most common spa types found in this study were associated with ST5 and expands the range of livestock-associated MRSA types.

MRSA in Conventional and Alternative Retail Pork Products

In order to examine the prevalence of Staphylococcus aureus on retail pork, three hundred ninety-five pork samples were collected from a total of 36 stores in Iowa, Minnesota, and New Jersey. S. aureus was isolated from 256 samples (64.8%, 95% confidence interval [CI] 59.9%–69.5%). S. aureus was isolated from 67.3% (202/300) of conventional pork samples and from 56.8% (54/95) of alternative pork samples (labeled “raised without antibiotics” or “raised without antibiotic growth promotants”). Two hundred and thirty samples (58.2%, 95% CI 53.2%–63.1%) were found to carry methicillin-sensitive S. aureus (MSSA). MSSA was isolated from 61.0% (183/300) of conventional samples and from 49.5% (47/95) of alternative samples. Twenty-six pork samples (6.6%, 95% CI 4.3%–9.5%) carried methicillin-resistant S. aureus (MRSA). No statistically significant differences were observed for the prevalence of S. aureus in general, or MSSA or MRSA specifically, when comparing pork products from conventionally raised swine and swine raised without antibiotics, a finding that contrasts with a prior study from the Netherlands examining both conventional and “biologic” meat products. In our study spa types associated with “livestock-associated” ST398 (t034, t011) were found in 26.9% of the MRSA isolates, while 46.2% were spa types t002 and t008—common human types of MRSA that also have been found in live swine. The study represents the largest sampling of raw meat products for MRSA contamination to date in the U.S. MRSA prevalence on pork products was higher than in previous U.S.-conducted studies, although similar to that in Canadian studies.

Methicillin-susceptible Staphylococcus aureus ST398, New York and New Jersey, USA.

To the Editor: Clinical infections with livestock-associated Staphylococcus aureus sequence type (ST) 398 have been reported in Europe, Canada, and the People’s Republic of China (1), as well as the Caribbean (2,3), and Colombia (4). Most reports describe infection with methicillin-resistant S. aureus; relatively few describe infection with methicillin-susceptible S. aureus (MSSA). In the United States, colonization of healthy adults by ST398 has been reported in Iowa (5) and in New York, New York (2); MSSA infections have been anecdotally reported in St. Louis, Missouri (6), and The Bronx, New York (7). We describe 8 infections with MSSA ST398 in the New York City area during a 7-year period (2004–2010). Five infections with a related ST (ST291) from clonal complex (CC) 398 also were identified. These findings highlight the emergence of clinical infections with 2 distinct CC398 sequence types in the New York City area. Retrospective typing of 4,167 clinical S. aureus isolates from various studies involving inpatients and outpatients in the New York City area identified 13 mecA-negative isolates with CC398-associated spa types (Table). Nine isolates were obtained from cultures of outpatients with skin and soft tissue infections; samples were submitted by physicians in the community. One isolate was associated with recurring skin and soft tissue infections in multiple body sites (BK21466); another was associated with genital infection (BK21732). Of the 4 ST398 isolates derived from bloodstream infections in hospitalized patients, 3 were recovered from intravenous drug users, 1 of whom died 1 day after admission for variceal bleeding (BK26722). Unlike the multidrug-resistant ST398 MSSA recently described in Colombia (4), most isolates in this study were susceptible to all antimicrobial drugs tested except penicillin, although several strains exhibited resistance to clindamycin and erythromycin. One isolate (BK23527) was submitted as oxacillin resistant (MIC ≥4 μg/mL) but lacked the mecA gene, which suggested that another mechanism was contributing to the resistance phenotype. Table Characteristics of Staphylococcus aureus clonal complex 398 isolates, New York and New Jersey, USA, 2004–2010* Multilocus sequence typing confirmed 8 isolates as ST398 (3–35–19–2–20–26–39); 5 isolates were assigned to ST291 (3–37–19–2–20–26–32), a double-locus variant of ST398 (Figure A1, panel A). Most of the ST398 strains were spa type 109 (t571), described in MSSA carriage isolates from New York City (2) and MSSA infections from China (1), France (8), Martinique (3), the Dominican Republic (2,3), and Colombia (4). BURP (based upon repeat pattern) analysis clustered all of the spa types into spa-CC t571 (Figure A1, panel B); ST398 isolates clustered with spa type 109 (t571), whereas ST291 isolates clustered with spa type 865 (t2313). Pulsed-field gel electrophoresis was also performed on the 11 available isolates. Although the ST291 isolates were sensitive to digestion with SmaI, pulsed-field gel electrophoresis was performed with Cfr9I to compare all isolates simultaneously. As expected, the ST398 and ST291 isolates clustered separately (data not shown); 4 distinct patterns were observed within each cluster (Table). Only the ST398 isolates were positive for a CC398 lineage-specific PCR that targets the unique restriction-modification system sau1-hsdS1 (9), further highlighting the differences between ST291 and ST398. None of the isolates harbored the genes coding for Panton-Valentine leukocidin. Because of the retrospective nature of the findings, epidemiologic information for each isolate was limited. One patient (BK19382) reported travel to the Dominican Republic; Caribbean nationality was reported for BK27037 (Puerto Rico) and BK31274 (Trinidad). The cases described here occurred in urban and suburban settings, reflecting the likelihood that exposure to livestock was relatively low; however, travel history was unknown for most of the patients. Previous reports have linked ST398 transmission to other reservoirs, including companion animals, live animal food markets, and commercial meat products (1,2). However, data from a recent genome sequencing study suggest that MSSA ST398 is human in origin (10); other evidence suggests that certain lineages, particularly spa type 109 (t571), might circulate at low levels in humans in the absence of livestock exposure (8). Our findings seem to support the hypothesis of low-level ST398 MSSA prevalence, and further surveillance might uncover additional cases of colonization or infection with ST398- and ST291-related strains in the New York City area. For example, active surveillance cultures performed at one of the 3 hospitals during January–March 2009 detected 7 additional ST398 and 3 additional ST291 isolates among 260 MSSA carriage strains (data not shown). In addition to the intrinsic virulence exhibited by ST398 MSSA in previous studies, the potential to acquire resistance to multiple classes of antimicrobial drugs (1,4,10), as well as virulence factors such as Panton-Valentine leukocidin (8), warrants continued surveillance in light of recent ST398 methicillin-resistant S. aureus outbreaks in health care settings (1).

Emerging Swine Zoonoses

The majority of emerging infectious diseases are zoonotic in origin. Swine represent a potential reservoir for many novel pathogens and may transmit these to humans via direct contact with live animals (such as swine farmers and large animal veterinarians), or to the general human population via contaminated meat. We review recent emerging microbes associated with swine and discuss public health implications.

Swine Farming Is a Risk Factor for Infection With and High Prevalence of Carriage of Multidrug-Resistant Staphylococcus aureus

BACKGROUND Livestock-associated Staphylococcus aureus (LA-SA) has been documented worldwide. However, much remains unknown about LA-SA colonization and infection, especially in rural environments. METHODS We conducted a large-scale prospective study of 1342 Iowans, including individuals with livestock contact and a community-based comparison group. Nasal and throat swabs were collected to determine colonization at enrollment, and skin infection swabs over 17 months were assessed for S. aureus. Outcomes included carriage of S. aureus, methicillin-resistant S. aureus (MRSA), tetracycline-resistant S. aureus (TRSA), multidrug-resistant S. aureus (MDRSA), and LA-SA. RESULTS Of 1342 participants, 351 (26.2%; 95% confidence interval [CI], 23.8%-28.6%) carried S. aureus. MRSA was isolated from 34 (2.5%; 95% CI, 1.8%-3.5%) and LA-SA from 131 (9.8%; 95% CI, 8.3%-11.5%) of the 1342 participants. Individuals with current swine exposure were significantly more likely to carry S. aureus (prevalence ratio [PR], 1.8; 95% CI, 1.4-2.2), TRSA (PR, 8.4; 95% CI, 5.6-12.6), MDRSA (PR, 6.1; 95% CI, 3.8-10.0), and LA-SA (PR, 5.8; 95% CI, 3.9-8.4) than those lacking exposure. Skin infections (n = 103) were reported from 67 individuals, yielding an incidence rate of 6.6 (95% CI, 4.9-8.9) per 1000 person-months. CONCLUSIONS Current swine workers are 6 times more likely to carry MDRSA than those without current swine exposure. We observed active infections caused by LA-SA. This finding suggests that individuals with livestock contact may have a high prevalence of exposure to, and potentially infection with, antibiotic-resistant S. aureus strains, including LA-SA strains.

Prevalence, antibiotic resistance and molecular characterisation of Staphylococcus aureus in pigs at agricultural fairs in the USA

Fairs and petting zoos have been associated with outbreaks of zoonotic disease. Previously, the presence of meticillin-resistant Staphylococcus aureus (MRSA) was documented in commercial pigs; therefore, it was hypothesised that antibiotic-resistant S aureus may also occur in pigs exhibited at agricultural fairs. To test this hypothesis, 157 pigs were swabbed at two state fairs in 2008 to 2009. Both nares were sampled and cultures were grown in enrichment broth, then plated onto selective MRSA plates and blood plates. S aureus was confirmed using phenotypic and molecular methods, and was analysed using spa typing, gene-specific polymerase chain reaction and antibiotic susceptibility testing. The presence of S aureus was confirmed in samples collected from pigs exhibited at USA pig shows. Twenty-five of 157 (15.9 per cent) samples were positive for S aureus. Two isolates (8 per cent) were resistant to meticillin; 23/25 (92 per cent), 14/25 (56 per cent) and 15/25 (60 per cent) were resistant to tetracycline, erythromycin and clindamycin, respectively. spa typing revealed multiple isolates of spa type t034 (9/25, 36 per cent) and t337 (7/25, 28 per cent) and singletons of t002, t209, t526, t1236, t1334, t1683, t3075, t5784 and t5883. These results verify the presence of antibiotic-resistant S aureus in pigs exhibited at USA fairs, suggesting that pigs are a potential reservoir for S aureus within this environment.

An Overview of Livestock-Associated MRSA in Agriculture

ABSTRACT Researchers, veterinary and health care practitioners, and agricultural producers gathered in Johnston, Iowa, to attend the eighth annual Midwest Rural Agricultural Safety and Health Forum (MRASH), November 2009. Among several focus areas, four plenary talks were given on the current research being conducted examining methicillin-resistant Staphylococcus aureus (MRSA) on swine farms in the United States. These focused on prevalence of MRSA on farms, both in swine and in human workers; the presence of MRSA in air samples and in swine barn shower facilities; and the presence of methicillin-resistant and methicillin-sensitive S. aureus in retail meats. These findings begin to elucidate the overall picture of livestock-associated MRSA in the Midwestern United States.

Methicillin-Resistant Staphylococcus aureus in Pork Production Shower Facilities

ABSTRACT As methicillin-resistant Staphylococcus aureus (MRSA) has been found in pigs, we sought to determine if MRSA is present in pork production shower facilities. In two production systems tested, 3% and 26% of shower samples were positive for MRSA. spa types identified included t034, t189, t753, and t1746.

Molecular and epidemiologic predictors of Staphylococcus aureus colonization site in a population with limited nosocomial exposure

BACKGROUND The anterior naris has been considered the most consistent location of asymptomatic Staphylococcus aureus colonization. However, recent studies have shown that a substantial number of individuals, ranging from 7% to 32% of colonized individuals, are exclusive throat carriers. Most of these studies have been carried out in a health care setting, limiting their generalizability to nonhospitalized populations. METHODS To evaluate anatomic carriage sites of S aureus in individuals outside of a health care setting, we combined the results of 2 cross-sectional studies conducted in Iowa. RESULTS S aureus was carried by 103 of 340 individuals (30.3%), including 31 (30.1%) exclusive throat carriers, 44 (42.7%) exclusive nose carriers, and 28 (27.2%) colonized in both sites. Nonwhite race (adjusted odds ratio [OR], 4.91; 95% confidence interval [CI], 1.26-18.3) and younger age (≥30 years: OR, 0.23; 95% CI, 0.10-0.54) were associated with increased odds of exclusive throat carriage, whereas nonwhite race (OR, 5.14; 95% CI, 1.62-16.3) and spring or summer sampling season (OR, 2.62; 95% CI, 1.32-5.18) were associated with increased odds of exclusive nasal carriage. CONCLUSIONS These findings suggest that including a throat swab in addition to a nasal swab could play an important role in the success of surveillance programs, particularly among younger adults.