The Occurrence of Antibiotic Resistant Bacteria in Manure, Manure-Applied Fields, and Pets on the Farm

Project Overview

LNC02-214
Project Type: Research and Education
Funds awarded in 2002: $99,835.00
Projected End Date: 12/31/2003
Region: North Central
State: Minnesota
Project Coordinator:
Dr. Satish Gupta
University of Minneota

Annual Reports

Commodities

  • Agronomic: corn, soybeans
  • Animals: bovine, swine, poultry

Practices

  • Animal Production: manure management
  • Crop Production: organic fertilizers, conservation tillage
  • Education and Training: extension, on-farm/ranch research
  • Soil Management: soil analysis

    Abstract:

    There was greater prevalence of antibiotic resistance bacteria (ARB) in manure from farms that use antibiotics sub-therapeutically than the farms that do not. This was more so for tetracycline than for tylosin or monensin. The trend was present for all three animal species; swine, turkeys, and cattle. However, this resistance did not appear to permeate to manure applied fields or dogs. Lack of trend in soil and dog fecal samples may be due to large variability (small number of farms). Resistance profile of ARB isolates from farms that use antibiotics sub-therapeutically showed higher levels of resistance to 20 other antibiotics.

    Introduction:

    Since their discovery, antibiotics have been instrumental in treating infectious diseases that were previously known to kill humans and animals. However, it has now become clear that widespread use of antibiotics is not without problems (Halling-Sørensen et al., 1998; Jørgensen and Halling-Sørensen, 2000). The major concern is the development of antibiotic-resistant microorganisms, which are difficult to treat with existing antibiotics (Ford, 1994; Herron et al., 1997). Furthermore, increasingly more microorganisms are becoming resistant to multiple antibiotics (Goldburg, 1999).

    According to one estimate, two million pounds of antibiotics were produced in the U. S. in 1954 compared to more than 50 million pounds being produced each year currently (Environmental Media Services, (EMS) 2000). Although most of these antibiotics are used for the treatment of infections in humans and animals, a significant portion is used as a supplement in animal feed to promote growth of food-producing animals. According to the Institute of Medicine, 32% of the antibiotics produced in the U.S are used as feed supplements (Shea, 2003). However, Union of Concerned Scientists (2001) contends that as much as 78% of the antibiotics produced are being used for non-therapeutic purposes in agriculture. The use of antibiotics in animal feed helps increase the animal’s ability to absorb feed and thus reach market weight quicker. In addition, supplementing antibiotics in animal feed counteract the effects of crowded living conditions and/or poor hygiene in intensive animal agriculture (EMS, 2000).

    Antibiotics commonly used as feed additive for animals include aureomycin, bacitracin, bambermycins, erythromycin, lincomycin, monensin, oxytetracycline, penicillin, tylosin, and virginiamycin (Church and Pond, 1982). The antibiotic dose varies from 1 to 200 g per ton of feed depending upon type and size of the animal and the type of antibiotic (Kumar et al., 2005). Most of the antibiotics added to animal feed are excreted in urine and manure, and as much as 80% may pass through the animal unchanged (Levy, 1992). Several groups contend that sub-therapeutic use of antibiotics in animal production is leading to increased presence of antibiotic resistant microbes in the environment including manure, soil, and water (Levy, 1992; Union of Concerned Scientists, 2001; Shea et al., 2001).

    Land application of manure is a common practice in many parts of the U.S. With emphasis on sustainable farming and demand for organic foods, there is even greater use of manure in current food production. The manure is land applied mainly because of its value in supplying nutrients to crops but in some cases it is also a means of disposing unwanted waste. According to Environmental Defense (2001), nearly 1 billion tons of animal waste is produced each year in the United States. Once land applied, the presence of antibiotics and antibiotic resistance bacteria in manure can cause selection of antibiotic resistance bacteria (ARB) in soil.

    Ability of pathogens to counteract the effectiveness of antibiotics leads to higher medicare costs. For example the cost of treating a patient with tuberculosis increases from $12,000 for a patient with a drug-susceptible strain to $180,000 for a patient with a multidrug-resistant strain (www.cspinet.org). In a report prepared by the U.S. Congressional Office of Technology Assessment (1995), it was concluded that the antibiotic resistance of just six different strains of bacteria has increased hospital costs by 1.3 billions in 1992 dollars.

    The groups most affected by continuous increased antibiotic resistance in microbes are the infants and children, senior citizens, and cancer, HIV/AIDS, and organ transplant patients (Shea et al., 2001). This is because their immune system is not fully developed or they have a weak immune system and thus need a full range of antibiotics to ward off infections.

    The goal of this study was to determine the role of sub-therapeutic feeding of antibiotics in food animals on increased microbial resistance in manure, soil where manure has been applied, and pets on the farm. The premise underlying the inclusion of pets in this study is to assess the potential spread of ARB to rest of the environment including humans on the farm.

    LITERATURE REVIEW

    About two years ago, antibiotics were found in a lake in Ohio (News Report on a TV Network, Feb. 2000). It is unknown how these pharmaceuticals found their way to the surface water. A possible route may be that antibiotics came to the lake with surface runoff from fields where manure had been applied. In 2003, there has been a comprehensive report on the National Public Radio (http://americanradioworks.org/features/farm/antibiotics.html) about the use of antibiotics in animal production and public’s concern about this practice. Because of the recent anthrax terror, there is also heightened awareness of regular antibiotic use in animal production and its consequences (Hilts, 2001, http://www.nytimes.com). Since manure, soil, and ground and surface waters are not regularly tested for antibiotics in the U.S., it is unknown to what extent this type of contamination exists in manure, soils, lakes, rivers, and groundwater in the United States.

    Some data are available on the occurrence, fate, and effects of pharmaceutical in the environment (Strauch 1987; Halling-Sorensen et al., 1998; Kumar et al., 2005). However, most of this work has been done in European Union countries and some of this literature is contradictory. Much of the concern has been related to pathways through which these pharmaceutical drugs find their way to the environment and their adverse effects on biological signals and the genetic structure of the ecosystem (Jørgensen and Halling-Sørensen, 2000). Another major concern is that widespread use of antibiotics may lead to new strains of bacteria that are resistant to these and other antibiotics and in turn result in untreatability of livestock diseases (Solomons, 1978; Hirsh and Wiger, 1977). During the 15 years period from 1975-1991 incidences of methicillin resistant Staphylococcus aureus (MRSA) isolates in U.S. hospitals has increased from 2.4% to 29% (www.cspinet.org). A potentially more dangerous scenario is the possible transmission of such strains to humans resulting in untreatable human diseases. Once land applied, the presence of antibiotics and antibiotic resistant microbes in manure can further lead to selection and propagation of ARB in the terrestrial environment and then to rest of the environment through non-point source pollution.

    Potentially, there are three mechanisms through which antibiotic resistance might develop in bacteria in the environment: (i) Continuous pressure from sub-therapeutic feeding of antibiotics leading to selection of ARB in the guts of animals, (ii) Microbes might acquire antibiotic resistance in-situ when antibiotic laced manure is applied to farms on a continuous basis, and (iii) Transfer of antibiotic resistance genes through genetic elements such as plasmid, integrons, transposons from ARB to sensitive bacteria. Potentially, one or all three mechanisms can act together to affect the prevalence of antibiotic resistant microbes in the environment.

    The limiting data on the spread of antibiotic resistance from animals that have been fed sub-therapeutic levels of antibiotics to the environment is generally conflicting. Nijsten et al. (1996a, b) reported that E. coli resistance was significantly lower in pig farmers than their pigs and the evidence for a common pool of plasmids among pig farmers and their pigs was inconclusive. Hunter et al. (1994) found a widespread dissemination of apramycin resistant plasmids in E. coli between the pigs and the stockman. These authors even found apramycin-resistant Klebsiella pneumoniae from the stockman’s wife despite the fact that she had no direct contact with the pigs. Earlier Hunter et al. (1992) reported on the possible transfer of apramycin-resistant plasmids from E. coli to Salmonella typhimurium in calves.

    With the recent availability of gene tracing techniques, there has been stronger evidence on the spread of antibiotic resistance from animal farms to the environment. Chee-Sanford et al. (2001) showed that there was some transfer of tetracycline resistance gene from manure lagoons to indigenous microbiota at two swine farms in Illinois. These authors also concluded that tetracycline resistance determinants were seeping into underlying groundwater as far as 250 m downstream from the lagoons. Based on the resistance patterns of E. coli in turkeys, turkey farmers, and turkey slaughterers and in broiler, broiler farmers, and broiler slaughterers, van den Bogaard et al. (2001) showed a strong indication on the transmission of resistant clones and resistant plasmids from poultry to humans.

    Perhaps a most comprehensive overview of this problem has come from The Committee on Drug Use in Food Animals from the National Research Council (1999). The Committee concluded, in part, that “a data driven scientific consensus on human health risk posed by antibiotic use in food animal is lacking”. The authors of this report recently put together a comprehensive review on the antibiotic use in agriculture and its impact in the terrestrial environment (Kumar et al., 2005). A copy of that review is attached with this report.

    Project objectives:

    The objectives of this study were: (1) to quantify the extent of antibiotic resistant bacteria in manure and manure-applied fields for three different types of animal (swine, beef, and turkeys) production systems, (2) to determine whether or not microbial antibiotic resistance is higher from farms that use sub-therapeutic levels of antibiotics (AU) vs. farms that do not use sub-therapeutic levels of antibiotics (NAU), (3) to assess whether microbial antibiotic resistance permeates to domestic pets that live on these farms, and (4) to identify manure and soil management practices that may lessen the impact of antibiotic use on antibiotic resistance in microbes on the farm.

    Any opinions, findings, conclusions, or recommendations expressed in this publication are those of the author(s) and do not necessarily reflect the view of the U.S. Department of Agriculture or SARE.