How under-testing of ethnic meat might contribute to antibiotic environmental pollution and antibiotic resistance: tetracycline and aminoglycoside residues in domestic goats slaughtered in Missouri.

Author:Landfried, Lauren K.


Antibiotic resistance results in over 2 million illnesses and 23,000 deaths yearly in the U.S. in addition to $20 billion a year in healthcare costs and $35 billion in lost productivity (Centers for Disease Control and Prevention [CDC], 2017; Marshall & Levy, 2011). Agriculture accounts for nearly 80% of antibiotic use (Food and Drug Administration [FDA], 2014a; The Pew Charitable Trusts, 2013) and has been well documented as a source of environmental and food pollution (Martinez, 2009), and a source of resistance genes in human pathogens, particularly enteric bacteria (Awad et al., 2015; Chang, Wang, Regev Yochay, Lipsitch, & Hanage, 2015; Marshall & Levy, 2011).

Antibiotics for food animals can be purchased and administered without direct veterinary oversight, and there is still a widespread but erroneous perception that continuous administration at subtherapeutic levels helps animal growth (Aarestrup, 2012). The Food and Drug Administration (FDA) has issued multiple recommendations to cease this practice (FDA, 2012), but it has continued nevertheless. Resistant bacteria are not only a public health issue with multiple potential routes of exposure aside from handling and consuming contaminated meat, including through the water supply and crops (Senta, Terzic, & Ahel, 2013), and they also pose an occupational hazard to farm workers (Gilchrist et al., 2007).

Through the National Antimicrobial Resistance Monitoring System (NARMS) with the Centers for Disease Control and Prevention (CDC) and the U.S. Department of Agriculture (USDA), FDA monitors only retail chicken, turkey, beef, and pork for contamination with resistant enteric bacteria Salmonella, Campylobacter, E. coli, and Enterococcus (FDA, 2014b). In its 2014 report, FDA found that 9.1% of chicken, 5.5% of ground turkey, 0.8% of beef, and 1.3% of pork samples tested at retail outlets were positive for Salmonella, with 60% of chicken and 70% of turkey strains resistant to at least one antimicrobial. Campylobacter, which causes an estimated 1.3 million illnesses and 120 deaths each year, was found in 33% of retail chicken samples (FDA, 2014b). Macrolide- and fluoroquinolone-resistant strains of Campylobacter jejuni, which account for 90% of morbidity and mortality due to Campylobacter, were detected in less than 4% and 15% of positive samples, respectively; antibiotic-resistant strains for Campylobacter coli were detected in 11-20% of retail chicken samples tested (FDA, 2014b). Prevalence of E. coli ranged from 43% in retail ground beef and pork chops to 83% in ground turkey, with rates of antibiotic resistance being highest in retail ground turkey at 83% and lowest in retail ground beef at 23% (FDA, 2014b). Enterococcus bacteria prevalence was quite high, ranging from 86-98% across all meats, with resistance rates >79% (FDA, 2014b).

In 2011, goat meat had the highest percentage of drug residues compared with other meat carcasses according to USDA's Food Safety and Inspection Service (FSIS) meat inspection results (USDA, 2013). This finding suggests that withdrawal times set for drug use in goats are not always followed or are imprecise because use of antibiotics in goats is predominantly extra-label, which means that drug dosages are extrapolated from those of other species rather than specifically tested in goats (National Milk Producers Federation [NMPF], 2016; Ruegg, 2013). At the time, USDA FSIS used only a two-tier approach to targeted testing: testing of suspicious animals at slaughter and herd-specific testing because of prior violations. In total, 346 samples (0.05%) were collected from 651,783 slaughtered goats, and 0.58% of these were positive for antibiotic residues (USDA, 2013). This rate of violation was greater than that of cattle and swine, which had a 0.19% violation rate with a 0.025% screening rate and a 0.01% violation rate with a 0.005% screening rate, respectively (USDA, 2013).

In 2012, USDA FSIS opted for an additional testing approach consisting of systematic sampling at slaughter for species making up 95% of the meat market, thus excluding goats (USDA, 2014). This new method yielded a 17fold increase in percentages of samples testing positive for antibiotics in these species, suggesting that adding systematic sampling to targeted sampling was likely to uncover more violations than targeted sampling alone.

Goat farming has increased significantly in recent years in response to consumer demand, but research on goat production in the U.S. is still relatively new. The National Agricultural Statistics Service (NASS, 2005) performed the first major survey of goat operations. Another study by USDA investigated the nation's goat industry in 2009 and focused on strategies for managing herds, such as seeking veterinary assistance, giving injections, knowledge of diseases, and sanitation after the birthing process (Animal and Plant Health Inspection Service, 2009).

These studies provided valuable insights on farming methods and farmer motivations, primarily that farmers who raised goats for meat had relatively little knowledge of antibiotics and withdrawal times, which is the FDA-mandated time between the last exposure to a specific medication and slaughter. The intent of withdrawal times is to avoid human exposure to antibiotics used to treat animals, either through meat handling or consumption.

Growing demand for goat meat in the U.S. over the past decade reflects an increase in ethnic immigrant populations and mainstream interest in the flavor and health benefits of goat products (Agricultural Marketing Resource Center, 2015; National Agricultural Statistics Service, 2015). In 2014, the immigrant population in the U.S. totaled 42.4 million with 30% coming from Asian and African countries, where 93.5% of the world goat production occurs (Anderson, 2017; Aziz, 2010; Food and Agriculture Organization of the United Nations, 2017; Migration Policy Institute [MPI], 2017; Zong & Batalova, 2017).

In Missouri, immigrants make up approximately 3.7% of the total population. Nearly half of those come from the high goat production areas of the world (MPI, 2017). From the public health standpoint, immigrants are considered a vulnerable population due to past lack of access to healthcare and lower socioeconomic status, which perpetuates some of these health inequities (Derose, Escarce, & Lurie, 2007). In 2014, 24% of U.S. immigrants lived below the federal poverty line compared with 15% of native-born U.S. citizens and fewer had health insurance than native-born U.S. citizens (53% compared with 68%) (Zong & Batalova, 2017).

The lack of precise drug dosages and withdrawal times for goats--combined with the inexperience of goat farmers in the U.S. regarding proper usage of these drugs, relative lack of attention from USDA on testing goat meat for antibiotic residues, exclusion of goat meat in the NARMS program, and rising goat meat demand by populations that often arrive in the U.S. with health vulnerabilities and have lower access to healthcare in this country--might amount to a brewing public health crisis in...

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