J. Lloyd Spencer and Jiewen Guan
During the 20th century, food animal agriculture grew from small operations, where livestock (cattle, sheep, and swine) and poultry (chickens and turkeys) had access to free range, to large operations where animals and poultry were concentrated and confined to feed lots or buildings. The quantity of manure produced by confinement animals in the United States has been estimated to be in excess of 61 million tons of dry matter per year (1), and another report states that 1.2 billion tons of manure are produced by cattle annually in the United States (US Senate Agricultural Committee, 1998). As urban developments have come closer to livestock operations, there has been increasing public concern for the impact of the latter on public health and the environment.
Although management practices for livestock production have increased in efficiency, insufficient attention has been given to managing and utilizing wastes so that they benefit rather than pollute the environment. Animal manure includes urine and various bodily secretions such as those from the nose, vagina, and mammary glands. Dust from animals and manure may be blown from buildings by powerful fans, and manure is often piled near the animal quarters or is spread on land in solid or liquid form. Public concerns associated with disposal of animal manure include objectionable odors, flies, excessive levels of phosphorous and nitrogen, and the potential for spread of human pathogens. It has been observed that despite linkages between outbreaks of gastroenteritis in humans and livestock operations, the importance of animal manure in the spread of infectious agents tends to be underestimated (2).
Slogans such as "farm to fork" and "plough to plate" have been used by the food industry to emphasize that food safety must begin on the farm. Technological advances aimed at the control of potential foodborne pathogens include the development of antimicrobial products, competitive exclusion products, and vaccines, along with improved methods for detecting infection or contamination in animals and their environment (3-5).
From: Methods in Molecular Biology, vol. 268: Public Health Microbiology: Methods and Protocols Edited by: J. F. T. Spencer and A. L. Ragout de Spencer © Humana Press Inc., Totowa, NJ
However, despite these advances, insufficient progress has been made in reducing the prevalence of potential foodborne pathogens on the farm. Poultry and other farm animals sold for slaughter frequently carry pathogens of human health concern to the killing floor of packing plants. Hazard analysis critical control point (HACCP) procedures have been implemented in killing and processing plants in an effort to prevent contamination of carcasses and meat with Salmonella and other foodborne pathogens. Although these measures have proven beneficial for reducing Salmonella contamination (6), once the equipment in the killing plant becomes contaminated, it is virtually impossible to prevent further contamination from occurring. In addition to contamination of meat, there is a concern for contamination of vegetables, fruits, spices, and water on the farm. Thus, to be successful in protecting food from contamination with pathogens, HACCP principles must also be more fully implemented on the farm.
Biosecurity is the term used with respect to livestock and poultry production to include measures that can or should be taken to prevent potential pathogens from gaining entrance to production facilities (7). However, despite the implementation of these measures, a high percentage of poultry and animal production facilities are contaminated with food- and waterborne pathogens. Many of these infectious agents persist on farms, and the practice of spreading raw manure on land is no doubt a contributing factor. Crops produced for animal feed as well as mice, flies, wild birds, dust, and water may become contaminated with pathogens in the environment and serve as vehicles to carry these agents back into animal quarters. Thus, biosecurity should include measures to prevent pathogens from exiting as well as entering animal facilities.
The following sections give further information on the relevance and spread of specific pathogens found in animal manure that could impact on human health. Measures that could be taken on farms to sanitize wastes and prevent environmental contamination are also considered.
2. Communicable Diseases Related to Management of Animal Manure
Animal manure has been found to be the source of more than 100 pathogens, including bacteria, parasites, and viruses, that could be transmitted from animals to humans (8). Many of these pathogens survive well in the environment and frequently persist in livestock operations. Infection of livestock and poultry with such pathogens may not produce clinical disease. In fact, animals act as asymptomatic carriers in amplifying the pathogenic agent that goes back into the environment in a cyclic manner. In most cases the producer would be unaware that the manure or bedding from animal quarters contains these pathogens. Since there is no official program in place to monitor animal manure and bedding routinely for pathogens of concern to public health, there is little incentive on the part of livestock producers to implement management practices to eliminate them from animal manure before it is spread on land.
Salmonella serotypes of food-safety concern are often referred to as paratyphoid Salmonellae. More than 2300 serovars have been described, and many infect warmblooded animals (3,9). Some of the serotypes of Salmonella frequently isolated from humans with symptoms of enterocolitis have been commonly detected in poultry meat.
In a US study, Salmonella enterica were isolated from 22.8% of the broiler chickens and from 1.8% of the beef carcasses (10). Salmonellosis may affect 1 to 5 million people each year in the United States (3). Rarely, Salmonella infection in humans leads to chronic conditions such as reactive arthritis, osteomyelitis, cardiac inflammation or neural disorders (11,12).
Young livestock and poultry are most susceptible to Salmonella infection, but usually the infected stock do not develop symptoms of disease. Infected stock, whether asymptomatic or sick, may shed high numbers of Salmonella organisms into the feces. It is not difficult to understand then that wastes from poultry and other animals, if not properly treated, can contribute to the spread of Salmonella (13). Surveys reported in 1991 found that the prevalence of Salmonella spp. was 52.9% in Canada's registered layer flocks and 76.9% in registered broiler flocks (14,15). Salmonella spp. were found in the manure from about 70% of the layer flocks surveyed in Southern California (16). In a survey in New York State, Salmonella organisms were isolated from poultry houses on all 28 farms included in the study (17). In one poultry house, S. enteritidis phage type 2 was isolated from chickens, manure, and mice. Other studies have shown that mice play a particularly important role in the epizootiology of Salmonella (18). In studies in Denmark, (19) S. typhimurium DT12 clone was found to have persisted in a piggery. The organism was isolated from waste slurry and from agricultural soil 14 d after slurry had been applied. It was suggested that contamination of soil could have been a factor in the persistence of the organism in the herd environment. A review article reported that Salmonella survived for 87 d in tap water, 115 d in pond water, 120 d in pasture soil, 280 d in garden soil, and 28 mo in naturally infected avian feces (20). These findings were in agreement with another review indicating that Salmonella survived for 9 mo in soil and for 3 yr in animal feces (21). Salmonella organisms have survived for 10 mo in slurry tanks of cattle manure and for 3 mo in soil after spreading of manure, plowing, and seeding (22). The fact that Salmonella organisms survive in the environment makes this pathogen a constant concern for poultry and livestock operations.
There is also growing concern over the emergence of antibiotic-resistant strains of Salmonella, and it is believed that widespread use of antibiotics in livestock production, for both preventative and treatment purposes, has contributed to the development of this problem. Although it is not known how the multiple antibiotic-resistant strain S. typhimurium DT 104 evolved, 37% of 323 isolations of salmonellae from swine in the United Kingdom in 1998 were this organism (21).
In addition to poultry and red meat, other sources of Salmonella are brought into domestic kitchens. Salmonella has been isolated from lettuce and other fresh vegetables, and large outbreaks of disease have been traced to eating cantaloupes and other fruits. It was suggested that the fruit may have become contaminated by irrigation with polluted water or by distributing products under poorly hygenic conditions (11). In experiments in which tomato plants were inoculated with salmonellae during the flowering stage, the organisms were found to survive in or on the developing fruits (23). This capacity to invade plant tissues indicates that simply washing and disinfecting produce may not be sufficient to eliminate Salmonella.
Campylobacter jejuni and C. coli are the species of Campylobacter most frequently implicated in foodborne infections. Infection in humans usually results in symptoms related to an enteritis, and about 2 million cases occur annually in the United States (24). A relationship has been found between intestinal infection with C. jejuni and the development of severe postrecovery autoimmune conditions including Guillain-Barre syndrome and Reiter's syndrome, a nonpurulent arthritis. The annual economic impact of Guillain-Barre syndrome in the United States was estimated to be $0.2-1.8 billion US, and about one-third of these cases were believed to be initiated by C. jejuni infection (25).
As is the case with Salmonella, food animals, especially poultry, are usually silent carriers of Campylobacter. Broiler flocks often shed the organism in feces from 2 to 3 wk of age onward. Thus it is not surprising that the organism has been isolated from a variety of environmental samples including rodents, wild birds, flies, feed, farmer's boots, and chicken feathers (26). Prevalence rates of Campylobacter infection among flocks have been reported to range from 18% in Norway to 90% in the United States (25). These wide differences in prevalence of infection between countries may be caused by the manure management practices and biosecurity measures that are practiced on farms (25,26). Campylobacter organisms can survive for several months in an aquatic environment but are susceptible to drying. There is a concern that some environmental stresses on the organisms may lead to viable nonculturable forms (25).
The high prevalence of infection with Campylobacter in poultry flocks has important public health implications. Humans may become infected by consumption of contaminated water or milk and meat products. Infection with C. jejuni has been an occupational hazard for poultry plant workers (25). The emergence of plasmid-medi-ated, antibiotic-resistant strains of Campylobacter has added to the health concerns (27).
Escherichia coli is a natural inhabitant of the intestinal tract of mammals and birds, and large numbers are shed in feces. In environmental monitoring programs, the number of E. coli in water is taken as an indicator of the level of recent fecal contamination and thus the potential presence of enteric pathogens. Although most of the E. coli strains found in environmental specimens are not long lived and are not pathogens, the cycling of this bacterium in animals and the environment could promote changes in the bacterial genome that could potentially increase virulence (28). In the early 1980s, E. coli O157:H7 emerged as a pathogen that could cause debilitating human illnesses and deaths. Syndromes in affected humans may include hemorrhagic colitis, hemolytic uremic syndrome, and thrombocytopenic purpura. Disease outbreaks in humans have usually been associated with ingestion of undercooked ground beef and raw milk. However, drinking water contaminated with E. coli O157:H7 has also been responsible for major outbreaks of disease (28).
Fruits, vegetables, and spices may also become contaminated with the organism on farms (2,29). Although contamination may be superficial, E. coli O157:H7 has been found to penetrate apple tissue (30). Also, it was found to enter lettuce plants through the root system and to survive in the plant tissues (31), thereby increasing the possibility for its persistence in environmental niches.
Dairy and beef cattle are the most important reservoirs of E. coli O157:H7, and large numbers of the pathogen may be found in bovine feces (21). In one study (32) in which E. coli O157:H7 was added to feces, the organism survived for up to 56 d at 22°C and for up to 70 d at 5°C. During these survival studies, isolates retained the ability to produce toxins that cause disease. Thus, unlike other strains of E. coli that are short lived, E. coli O157:H7 can survive in adverse environments and has been found to be very tolerant to changes in pH (21). The practice of spreading cow manure slurry on pastures has created an environment that favors the persistence of E. coli O157:H7 (33) and could be a source of infection for animals.
Sheep, cattle, pigs, and chickens and many other species of animals and birds are susceptible to infection with Listeria monocytogenes and shed the organism in their feces. L. monocytogenes is known for its ability to survive well in the environment, partly because of its ability to grow at temperatures as low as 4°C, an attribute not shared with the aforementioned enteric pathogens. The organism has been shown to be more resistant to changes in pH and to accumulations of ammonia in manure than were S. typhimurium and E. coli O157:H7, thus enhancing its environmental persistence (34). L. monocytogenes has been found in high numbers in poorly fermented silage, and this feedstuff has frequently been the source of the pathogen in on-farm outbreaks (21). In one such report, sheep fed corn silage developed listerial encephalitis, and losses from the disease stopped when feeding of the silage ceased (35).
On dairy farms, milking practices were shown to influence the odds of detecting L. monocytogenes in milk, and there was evidence that manure was the source of the contamination (36,37). On one Japanese farm (37), the organism was frequently isolated from milk and was also detected in manure and in soil on which the fodder plants were grown. Application of manure to the land may have led to contamination of fodder plants and subsequently to infection of cattle.
Humans have become infected with L. monocytogenes by eating raw vegetables that had been fertilized with sheep manure (2). Perinatal infections with this pathogen may cause a high rate of fetal mortality, and infections in immunologically compromised individuals may result in meningitis and death (38).
Cryptosporidium parvum is a protozoan parasite that infects cattle, sheep, horses, and pigs. Oocysts are the infectious stage of the parasite found outside the host; they may remain viable for several months (39). Since the oocysts are shed in feces, manure management practices have been a factor in spread of infection. A nationwide survey in the United States found that more than half of the dairy farms studied had calves that tested positive for infection with C. parvum, indicating a widespread distribution of infection. Although the infection was usually self-limiting, it was noted that infected neonatal calves could excrete 30 billion oocytes over a period of 2 wk
(40,41). Although animals acquired resistance with age, apparently healthy cows in one study were found to shed 18,000 oocysts/g of feces (42). The parasite has been shown to be resistant to a number of commercial disinfectants including the routine levels of chlorine used for treatment of public drinking water (43).
Humans become infected by drinking water or by swimming in recreational water contaminated with the pathogen. Usually, those infected develop a diarrheal illness, but in immunocompromised individuals, a chronic infection can develop and may be fatal. In a major outbreak in Wisconsin, 400,000 people, most of whom were healthy, became ill after they drank contaminated public water (44).
Influenza viruses are not considered to be foodborne pathogens, but the feces shed by infected birds may be a source of infection for humans (45). Influenza viruses belong to the Orthomyxoviridae family and are classified as type A, B, or C based on antigenic differences in nucleoproteins and matrix proteins. They are further subtyped based on the antigenicity of two surface glycoproteins known as hemagglutinin and neuraminidase. Wild aquatic birds are silent carriers of influenza viruses and are a source of infection to other animal species. As the influenza viruses spread among birds and animals, there is a possibility for mutations and for exchanging of genetic material among these viruses that may lead to emergence of strains that are pathogenic for humans. The H1N1 virus, which caused the great pandemic of 1918-19, known as Spanish influenza, resulted in more than 20 million human deaths (46).
Viruses that cycle in avian populations are of type A and are usually no threat to human health. However, in 1997, an H5N1 virus that had circulated in Hong Kong's poultry population caused 18 cases of severe respiratory illness and 6 fatalities in humans. Previously, H5 viruses had only been isolated from the avian species. In the outbreak, all internal genes, including those that encoded the surface glycoproteins, were of avian origin. This was evidence that the H5N1 virus from poultry had crossed the species barrier (47). However, it has been suggested that H9N2 virus may have provided replicating genes for H5N1 (48). H9N2 viruses had been isolated in the Hong Kong area from poultry, pigs, and humans. It is important to note that small farms that sell poultry through live bird markets tend to keep multiple species of birds and animals. The movement of stock, crates, and vehicles to and from the markets would favor spread, multiplication, and mixing of influenza viruses. Thus live bird market operations are a potential reservoir for influenza viruses of concern to animal and public health.
In the 1997 Hong Kong outbreak, the human index case occurred in May, and there were no further cases until November of that year. Presumably there was a buildup of virulent virus in the poultry population between those months. It has been suggested that slaughter of all poultry in Hong Kong may have averted the continued spread of the disease to humans. What happened in Hong Kong may be analogous to what has occurred in outbreaks of highly pathogenic avian influenza in large commercial poultry operations. Typically, in those outbreaks low virulent viruses circulate in the population and then a highly virulent mutant emerges. This was the case in an outbreak in
Pennsylvania in 1983. In April of that year an avirulent H5N2 influenza virus appeared in poultry populations, and then in October of the same year, a highly virulent virus emerged that caused more than 80% mortality in some flocks. In the eradication effort, over 17 million chickens and turkeys were destroyed at a cost of over $61 million. Analyses indicated that genes of the virulent virus were derived from an avirulent virus (46).
Influenza viruses multiply in the respiratory and intestinal tract, and large numbers of virus particles may be excreted in the feces of infected birds. It was noteworthy that the H5N1 virus that caused disease in humans had been detected in bird feces in poultry markets in Hong Kong. Studies on stability showed that infectivity of H5N1 was lost within 1 d in feces dried at room temperature. However, when feces was kept moist at 25°C, the virus was detectable after 4 d, and at 4°C there was no detectable loss in moist feces after 40 d (45). Although airborne transmission of influenza viruses occurs, it has been shown that the fecal-oral transmission of H5N1 was more common (48). Fecal contamination of water would be expected to be important in the perpetuation of infection in waterfowl and shore birds and may also contribute to the spread of disease to humans. In addition, fecal contamination of poultry meat would also be a potential source of infection for humans. All these observations on the stability and spread of influenza viruses in manure indicate that farm waste management practices should be an important consideration in the prevention and control of this disease.
3. Composting for Elimination of Pathogens From Animal Wastes
As noted above, many pathogens of public health concern may be found in large numbers in animal manure. The more microorganisms such as E. coli and influenza viruses pass from animal to animal and from species to species, the greater is the likelihood for mutants to emerge with undesirable properties such as increased virulence and, in the case of bacteria, increased resistance to antimicrobial products (28,48). Thus, implementing manure management practices, in order to eliminate pathogens from animal wastes before land application, could greatly reduce the spread of disease to animals and humans.
In crisis situations such as outbreaks of S. enteritidis or influenza, the decision might be made to depopulate the animal premises. In such cases, measures should be taken to dispose of animals and manure safely. However, in practice, the importance of microbes in manure appears to be given lower priority than those in carcasses (2). In some cases carcasses may be burned to ashes to ensure complete destruction of pathogens, whereas manure from these animals, laden with the same pathogen, may be spread directly on land. The recommendation to plow the field within 24 h of applying the contaminated manure, in order to discourage birds and other scavengers (49), seems inadequate.
In addition to crisis situations, waste management continues to be a concern in routine livestock production. With the intensification of management practices, many producers have adopted slurry systems for the disposal of manure. A study in Sweden (22) reported that the spread of salmonellae in herds of cattle was greater on farms using slurry systems than on those using solid manure systems. This was attributed in part to the killing of salmonellae by heat generated in piles of manure. The traditional manure pile, consisting of a mixture of moist manure and bedding, is a crude compost pile, but conditions are not suitable for thoroughly sanitizing the wastes. The interior of such piles may reach temperatures sufficient to kill pathogens, but the exterior may be close to ambient temperatures and may favor survival of Salmonella and other pathogens (16,49).
A properly designed and managed composting operation has the potential for eliminating animal and human pathogens from the entire compost pile consisting of manure, animal carcasses, and other organic wastes. Composting offers a safe, economical, and environmentally acceptable alternative for disposal of animal wastes (50,51). Systems can be designed to dispose of manure and carcasses together, and the end product can be spread on land as a soil amendment. Although it is possible to compost liquid manure (52), large quantities of bulking agent must be mixed in to bring the moisture content to an acceptable level. Temperatures of 55-60°C for 3 d have been sufficient for killing most pathogens in compost (21,53). In addition to heat, enzymatic activity and ammonia production may also contribute to the sanitizing process during composting, and it was suggested that the action of composting lowered the temperature required to kill certain plant pathogens (54). Thermotolerant mutants of Salmonella and E. coli have been developed under laboratory conditions (55), but there appears to be no evidence that such mutants have emerged and caused problems in the environment during millenia of composting.
Chicken manure has been composted in high-rise cage layer barns in an effort to control flies (56). In those studies, manure was mixed with wheat straw, and the biomass reached temperatures of at least 43°C. When the biomass was turned, the temperatures rose to about 60°C and then rapidly declined. Although temperatures achieved were sufficient to control flies, temperatures of 55-60°C were not maintained long enough to ensure the killing of pathogens. This suggests the need for an improved composting design to conserve heat.
Like manure piles, some of the methods that have been developed for composting animal carcasses may not ensure complete sanitization of wastes. Sheep carcasses have been composted in bins that were filled with layers of barley straw, cured compost, dead sheep, and manure (57). In other studies, animal carcasses were buried in sawdust (50,58). In these operations the outer surfaces of the mass in the primary bins would not reach temperatures sufficient to kill pathogens. However, if contaminated materials were placed toward the center of the piles, the risk of spreading pathogens would be reduced. In addition, when the temperature declines in primary bins, transfer of the mass to secondary bins would cause a resurgence of heat production that would further reduce levels of viable pathogens. Measures that can be taken to make composting of farm animals a safe and acceptable alternative to burning or burying have been reported (51).
A static pile, passive aeration system has been used to compost manure and fish wastes (52,59). Compost piles were built over aeration pipes and remained static until the compost had matured. Since turning of the compost was not necessary to provide aeration, the system could have advantages for disease control. Using this system, compost piles were prepared that were composed of chicken litter contaminated with S. typhimurium. The Salmonella was eliminated toward the center of the piles within 10 d of composting but persisted at the surface. In subsequent studies, piles were covered with a vapor barrier fabric and then insulation was laid over the fabric. The fabric conserved moisture needed for microbial activity within the piles and protected the overlying insulation from becoming contaminated. Sufficient heat was generated throughout the entire compost pile to kill Salmonella and other pathogens (Spencer, unpublished data).
Anaerobic digestion of animal manure has been used for biogas production, and it appears that toxic substances produced during this process may kill pathogens. It is also possible to compost the anaerobically digested materials to complete the sanitiza-tion process (54).
Air quality inside animal facilities is influenced by such factors as temperature, humidity, air circulation, and manure management practices. A buildup of dust or ammonia and other odorous chemicals in animal quarters can render animals more susceptible to disease. Many infectious agents are carried on dust particles and can travel several miles through the air. For example, in areas of high-density poultry production, virtually all flocks must be vaccinated against a number of important virus diseases, yet nonvaccinated chicks can be kept free of these and other diseases if they are raised in buildings where all air entering the facility passes through HEPA filters (60,61). These so-called filtered air positive pressure (FAPP) houses are now routinely used for production of the specific pathogen-free chickens required for research and production of biologicals. Although FAPP facilities have been considered too costly to be used by the commercial poultry industry, their effectiveness in preventing entrance of disease-causing organisms has shown the importance of air in the transmission of disease.
Biofilters have been designed for removing odors from air exiting livestock facilities (62), and it is likely that these filters also remove some pathogens. Research is needed to develop biofilters or other systems to remove pathogens efficiently from air exiting animal production buildings.
In conclusion, public health problems associated with the food- and waterborne pathogens appear to have grown with the poultry and livestock industries. However, the notion that salmonellae are ubiquitous in the natural environment should be qualified (11). Large poultry breeding companies have demonstrated that chickens can be raised totally free of Salmonella and other zoonotic pathogens (4). The added costs to producers of developing and implementing composting and other practices to prevent pathogens from exiting and entering animal quarters may be more than compensated for by reduced losses from diseases. In addition, public health would benefit. Proactive measures to prevent environmental pollution from agricultural operations could make it more acceptable for large production operations to be developed closer to urban centers, resulting in further economic benefits.
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