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REVIEWS AND ANALYSES

Pathogen Survival in Swine Manure Environments and Transmission of Human Enteric Illness—A Review

Department of Food Science, Faculty of Agricultural and Food Sciences, Univ. of Manitoba, Winnipeg, Manitoba, R3T 2N2 Canada

^* Corresponding author (rick_holley{at}umanitoba.ca)

Received for publication May 14, 2002.

	ABSTRACT

TOP NOTES ABSTRACT INTRODUCTION MANURE HANDLING AND FOODBORNE... EFFECT OF INCREASED HOG... ENVIRONMENTAL SURVIVAL OF THE... CONCLUSIONS REFERENCES

 
The influence of zoonotic pathogens in animal manure on human health and well-being as a direct or indirect cause of human enteric illness is examined. Available international data are considered, but the study is focused on the developing situation in western Canada, where it is certain there will be further rapid growth in livestock numbers, particularly hogs. Major pathogens considered are Escherichia coli O157:H7, Salmonella, Campylobacter, Yersinia, Cryptosporidium, and Giardia. Canada is now the leading exporter of pork internationally, but recent increases in production contrast with constant domestic levels of pork consumption and declining levels of foodborne illness caused by pork. Effects of increased levels of manure production are not quantifiable in terms of effects on human health. The presence of major pathogens in manure and movement to human food sources and water are considered on the basis of available data. Survival of the organisms in soil, manure, and water indicate significant variability in resistance to environmental challenge that are characteristic of the organisms themselves. Generally, pathogens survived longer in environmental samples at cool temperatures but differences were seen in liquid and solid manure. Based on actual data plus some data extrapolated from cattle manure environments, holding manure at 25°C for 90 d will render it free from the pathogens considered above.

	INTRODUCTION

TOP NOTES ABSTRACT INTRODUCTION MANURE HANDLING AND FOODBORNE... EFFECT OF INCREASED HOG... ENVIRONMENTAL SURVIVAL OF THE... CONCLUSIONS REFERENCES

 
THIS REVIEW EVALUATES the survival of zoonotic-based protozoan and bacterial pathogens in soil, water, and manure. We focus on several aspects related to the issue, including improper manure handling and foodborne illness, the effect of increased hog production, and environmental survival of the major zoonotic pathogens from swine and cattle.

	MANURE HANDLING AND FOODBORNE ILLNESS

TOP NOTES ABSTRACT INTRODUCTION MANURE HANDLING AND FOODBORNE... EFFECT OF INCREASED HOG... ENVIRONMENTAL SURVIVAL OF THE... CONCLUSIONS REFERENCES

 
The danger of improper manure handling can be manifest as direct contamination of produce, water supplies, animals, or even humans. A summary of human enteric diseases where manure handling was implicated as the cause of infection is presented in Table 1. As shown in the table, manure application affects the safety of fresh produce and water supplies. Waterborne outbreaks and those associated with fresh produce have been on the rise in recent decades and will likely increase, in part due to increased surveillance. In most of these outbreaks the source of contamination was not confirmed. Although rarely identified as the cause, whenever manure was implicated in an outbreak, the results were serious (Table 1). In half of these outbreaks, mortality occurred. Since the source of contamination in most disease outbreaks is uncertain, the risks from improper manure handling are probably greatly underestimated.

Proper composting of manure can yield safe fertilizer. In Canada, regulations for treating animal manure are almost nonexistent. Farmers are provided with guidelines for storing and spreading manure; however, the guidelines are voluntary. Canadian commercial compost standards require that during windrow composting a temperature of 55°C or greater is maintained for at least 15 d during the composting period, and that during the period the compost is turned at least five times (Composting Council of Canada, 2002). For industrial composting systems where the process is closely monitored and controlled, consistent elimination of pathogens can be achieved. However, in many farm composting systems there is less control over the process and it is more difficult to ensure uniform exposure to high temperature, which may result in the survival of some pathogens (Patriquin, 2000). On the farm, there is also a likelihood of reintroduction of pathogens by sequential addition of new manure during the composting process. Allowing time for proper composting is critical. Two- to four-month composting times have been suggested for backyard composts to get rid of E. coli O157:H7 (Environmental News Network, 1997). Composting of manure is obviously important for its use on food crops, but may also be important for forage crops to reduce levels of E. coli O157:H7 in livestock. Escherichia coli O157:H7 is resident much longer in manure than in the live animals, and thus manure-contaminated materials are thought to be a source for reinfection of livestock with E. coli O157:H7 (Kudva et al., 1998).

Land application of raw manure also results in contamination of agricultural runoff and water supplies. Contaminated drinking water has the potential to cause extensive outbreaks due to the large populations served by many distribution systems. The Walkerton (Ontario, Canada) and Milwaukee (Wisconsin) outbreaks are two well-known examples. In Walkerton it was confirmed that human pathogens from cattle manure on adjacent farms entered the municipal water supply following heavy rains and flooding (Health Canada, 2000). The outbreak resulted in six deaths. In the Milwaukee outbreak, it was estimated that more than 100 deaths occurred over the two years following the massive outbreak there. Many of these were due to chronic complications, especially in immunocompromised persons (Hoxie et al., 1997).

The extent of water contamination in Canada due to agricultural practices has not been well studied. In one report it was found that bacterial contamination of surface water occurred at a single field site in Ontario due to liquid manure spread with accepted practices over a two-year period (Joy et al., 1998). Results showed that significant numbers of bacteria could reach the surface water by infiltrating through the soil and traveling through subsurface tile drains to the receiving water. Rainfall shortly after manure application was suggested to be the most important factor influencing bacterial contamination rather than spreading rate (volume applied per unit area) or condition of the field before spreading. Goss et al. (1998) examined well contamination problems resulting from the use of manure in Ontario, and reported that the number of wells showing bacterial contamination increased from 15 to 25% between 1955 and 1992. In Manitoba, early in the summer of 2000, the community of Balmoral in the regional municipality (RM) of Rockwood was advised to boil its drinking water. It was found that of the 75 wells serving the community, 86% contained coliform and/or E. coli bacteria (Canada–Manitoba Infrastructure Program, 2001a). In September 2000, another boil water advisory was issued for the community of Haywood in the RM of Grey in the province after the finding that 90% of 55 wells sampled were contaminated by bacteria (Canada–Manitoba Infrastructure Program, 2001b). However, the sources of contamination in both incidents were not determined.

In Manitoba, 23.6 million Mg of manure are produced annually, according to 1997 statistics (Manitoba Rural Water Quality, 1999). The largest single manure source in the province was cattle grazed on rangeland where manure is not collected. When manure production in Manitoba is broken down by livestock group, cattle and calves were responsible for 84.5%, hogs 14%, and others 1.5% (1997 data). Manure production will increase as the hog industry in the province continues to grow (Manitoba Rural Water Quality, 1999). Manitoba is the third largest hog producer in the country after Quebec and Ontario (Table 2). Most manure-associated outbreaks have implicated bovine manure more frequently than other types (Table 1). This has led to more study of pathogens in bovine than in hog manure. The amount of information on pathogens in swine manure is very limited. A study on Ontario livestock farms in 1996 (Fleming, 1999) found that Cryptosporidium appeared to be more prevalent in swine than in dairy manure. This study showed that 26% of all swine liquid manure samples tested positive for the protozoan, compared with 8.1% for dairy solid manure and 7.3% for dairy liquid manure. For each of the three farm types (swine farms with liquid manure, dairy farms with solid manure, and dairy farms with liquid manure), 50 to 55% of the farms tested positive for the protozoan at least once in the fresh manure (from young pigs or calves). In contrast, 75% of the swine farms with liquid manure storages tested positive at least once, compared with 20% of dairy farms with solid manure storages and none of the liquid dairy manure storages. The author's later study in 1998 on Ontario swine farms suggested that oocysts were present in about 50% of manure samples, and of those that tested positive, at least some viable organisms were present 60% of the time (Fleming, 1999).

View this table: [in this window] [in a new window]   Table 2. Hogs marketed in Canada by province, 1984–2000 (thousands of head).

	EFFECT OF INCREASED HOG PRODUCTION

TOP NOTES ABSTRACT INTRODUCTION MANURE HANDLING AND FOODBORNE... EFFECT OF INCREASED HOG... ENVIRONMENTAL SURVIVAL OF THE... CONCLUSIONS REFERENCES

View larger version (11K): [in this window] [in a new window]   Fig. 1. Incidents of pork-associated human enteric illness in Canada, 1975–1995. Data from Todd (1990)(1991), Todd and Harboway (1994), Todd and Chatman (1996)(1997, 1998), and Todd et al. (2000).

View larger version (12K): [in this window] [in a new window]   Fig. 2. Cases of pork-associated human enteric illness in Canada, 1975–1995. Data from Todd (1990)(1991), Todd and Harboway (1994), Todd and Chatman (1996)(1997, 1998), and Todd et al. (2000).

View larger version (16K): [in this window] [in a new window]   Fig. 3. Per capita disappearance of pork in Canada, 1982–2000. Data from Statistics Canada (2000)(2001). Does not estimate trim at wholesale and retail or table waste.

View larger version (15K): [in this window] [in a new window]   Fig. 4. Canadian hog production, 1982–2000. Data from Statistics Canada (2000)(2001).

View this table: [in this window] [in a new window]   Table 3. Foodborne outbreaks of human illness from pork in the United States, 1973–1992.

View this table: [in this window] [in a new window]   Table 4. Per capita pork consumption and pork production in the USA, 1992–2000.

	ENVIRONMENTAL SURVIVAL OF THE MAJOR ZOONOTIC PATHOGENS FROM SWINE AND CATTLE

TOP NOTES ABSTRACT INTRODUCTION MANURE HANDLING AND FOODBORNE... EFFECT OF INCREASED HOG... ENVIRONMENTAL SURVIVAL OF THE... CONCLUSIONS REFERENCES

 
The survival of several major zoonotic pathogens under different environmental conditions is summarized in Table 5. Predictions are made where data do not exist. In general, zoonotic pathogens appear to survive longer in water, followed by soil and manure. In each of these environments, they survive better at lower than at higher temperatures.

The fate of Salmonella species (including Salmonella enterica Typhimurium DT 104) in river water was examined by Santo Domingo et al. (2000). The authors inoculated river water and steam sterilized (autoclaved) river water with 8 log₁₀ colony forming units (CFU)/mL Salmonella. After 45 d at room temperature, they observed that the number of Salmonella was reduced by more than 3 logs in the untreated water while the number of these organisms was reduced by 2 to 3 logs in the treated water. However, when the VBNC cells were examined, less than 1 log of reduction was observed after 45 d in both types of water. Lengthy survival of Salmonella spp. in natural water was also recorded in Mitscherlich and Marth (1984), where a survival time of at least 152 d was noted in sterilized well water at 18 to 20°C. It is clear that Salmonella species can survive for a long period of time in natural water bodies, and possibly even longer at lower temperatures.

Yersinia enterocolitica is a psychrotrophic organism, which underlines its significance in refrigerated foods, where it can grow. Its lengthy survival in water was noted by Karapinar and Gonul (1991), who detected survivors in sterile spring water after 64 wk at 4°C. Survival was greatly reduced with increasing temperatures. For example, Chao et al. (1988) reported viable numbers after 6 d at 16°C in river water, and 10 d at 30°C in ground water. The difference was explained by the presence of eukaryotic predators and toxic materials (e.g., biological toxins, chemical toxicants), which are usually higher in surface water. Terzieva and McFeters (1991) also noted extended survival at reduced temperatures, with the pathogen surviving at least 14 d at 16°C.

In water, Campylobacter survived for 8 to 28 d at 4°C (Buswell et al., 1998; Terzieva and McFeters, 1991; Blaser et al., 1980). Survival times were similar at 16°C (Terzieva and McFeters, 1991) but were greatly shortened as the temperature increased to 22°C and above. At 22 and 37°C, the organism only survived for 43 and 22 h, respectively (Buswell et al., 1998). The VBNC state of Campylobacter jejuni in water was demonstrated by Rollins and Colwell (1986). They found that stream water held at low temperature (4°C) sustained significant numbers of VBNC C. jejuni for more than 4 mo.

Giardia cysts are much more susceptible to environmental stress than Cryptosporidium oocysts. A study by Olson et al. (1999) showed that temperatures as low as -4°C inactivated Giardia cysts in water while Cryptosporidium oocysts remained viable for >12 wk. At 4°C in water Giardia cysts were infective for 11 wk while Cryptosporidium oocysts again survived for >12 wk. At 25°C Giardia cysts were noninfective in water within 2 wk but Cryptosporidium oocysts were infective up to 10 wk.

In cold water (4 to 8°C), Y. enterocolitica has the greatest survival among all pathogens whereas Campylobacter has possibly the least. In warm water (20 to 30°C), Salmonella survives best, followed by E. coli O157:H7, Cryptosporidium, Giardia, Y. enterocolitica, and lastly Campylobacter.

Survival in Soil
Escherichia coli O157:H7 can survive in soil for a long period of time depending on the soil type. In the laboratory, the organism survived for at least 8 wk in moist soil at 25°C (Mubiru et al., 2000). Under fluctuating environmental temperatures (-6.5 to 19.6°C), the organism can be detected for up to 99 d (Bolton et al., 1999). Among the physical and chemical properties of soil, soil moisture is a major factor determining bacterial survival. Greater survival is often associated with moist soils, thus rainfall is a factor that favors bacterial survival.

Salmonella is relatively persistent in soil compared with other pathogens. When inoculated at 8 log₁₀ CFU/g into moist soil, which was then stored at 20°C, less than 2 log reductions were observed after 45 d (Guo et al., 2002). These findings are consistent with the results of an early study by Zibilske and Weaver (1978), who reported survival of Salmonella enterica Typhimurium in soil for 42 d at 22°C, and for 63 d at 5°C. Under natural environmental conditions, Salmonella enterica Typhimurium was isolated up to 14 d from agricultural soil amended with Salmonella-contaminated hog manure slurry, which was spread in spring (Baloda et al., 2001). The authors also cited their unpublished data, which showed that under controlled conditions in terrestrial ecosystems, Salmonella enterica Typhimurium DT 104 and DT 12 could survive up to 299 d, although the temperature was not noted.

In the laboratory, Y. enterocolitica survived for 7 d in soil at 30°C (Chao et al., 1988). Survival times could be prolonged to 10 d in pH-adjusted soil (final pH 6.5) and air drying of the pH-adjusted soil reduced the number of survivors. In an early study, Campylobacter intestinalis survived in nonsterilized soil for 20 and 10 d at 6°C and 20 to 37°C, respectively (Lindenstruth et al., 1949 cited by Mitscherlich and Marth, 1984).

While Giardia is sensitive to freezing of soil, Cryptosporidium is resistant. Olson et al. (1999) reported Giardia cysts in soil were noninfective after 7 d at -4°C, but Cryptosporidium could survive for >12 wk. Infective Giardia cysts and Cryptosporidium oocysts were recovered from soils maintained at 4°C for up to 8 wk. At 25°C, Giardia cysts were inactivated at 1 wk in soil whereas Cryptosporidium oocysts survived and were infective for 4 wk. Cryptosporidium oocysts were degraded more rapidly in soil containing natural microorganisms than in sterile soil (Olson et al., 1999). It has been suggested that soil sterilization destroys competing indigenous microflora, increases available nutrients for microorganisms, and reduces concentrations of inhibitory compounds unstable at treatment temperatures (Mitscherlich and Marth, 1984).

In cold (4 to 6°C) soil, most pathogens can survive for at least 30 d. Among all pathogens considered, the greatest survival was found for Cryptosporidium in frozen soil and E. coli O157:H7 and Salmonella in warm (20 to 30°C) soil (Table 5).

Survival in Manure
When exposed to fluctuating environmental conditions, E. coli O157:H7 could survive for more than 1 yr in nonaerated ovine manure (Kudva et al., 1998). In aerated ovine and bovine manure piles held in the natural environment, the organism survived for 4 mo and 47 d, respectively. Aeration was believed responsible for accelerating the drying of manure, and this probably resulted in the reduction of the number of pathogens (Kudva et al., 1998). Under controlled laboratory conditions, the pathogen survived for at least 100 d in bovine manure frozen at -20°C and 100 d in ovine manure incubated at 4 or 10°C. These results were in agreement with those of Wang et al. (1996), who also reported longer survival in manure (bovine) at lower temperatures. Their studies showed E. coli O157:H7 survived for 70 d at 5°C, 56 d at 22°C, and 49 d at 37°C.

Survival data for Salmonella spp. in various animal manures are reported in Mitscherlich and Marth (1984). In pig slurry, S. senftenberg survived for 14 d at 8°C, 8 d at 20°C, and <8 d at 37°C (Muller, 1973 cited by Mitscherlich and Marth, 1984). In cattle slurry, Salmonella enterica Typhimurium was not detectable after 19 d at 37°C, but survived for at least 60 d at 4 and 20°C (Himathongkham et al., 1999). In cattle manure, the organism survived for 48 d at 37°C. The authors observed an exponential linear destruction of Salmonella enterica Typhimurium and E. coli O157:H7 in cattle manure and manure slurry stored at 4, 20, or 37°C. The decimal reduction times (DRT; times required for 90% reduction) of the pathogens are presented in Table 6. The DRT values may be useful in risk assessments to predict how long manure should be held before application to fields. It appears that both pathogens survived less well in liquid manure than in solid manure at 20 and 37°C while the opposite was true at 4°C. Therefore, handling manure as a liquid may be a better alternative as less time is required to kill the pathogens. Further, greater survival occurred at 20 and 37°C in fresh manure slurry compared with old manure slurry (slurry made from manure that was stored for months and had become dried). This indicates that manure stored at warm temperatures for a period of time is an unfavorable environment for survival of the pathogens. This is probably because stressed microorganisms survive for shorter periods of time at warmer than cooler temperatures where metabolic rates are slowed (Montville and Matthews, 2001). In addition, these findings stress the importance of spreading manure to fields only during warmer months.

View this table: [in this window] [in a new window]   Table 6. Decimal reduction time (DRT) values of Escherichia coli O157:H7 and Salmonella enterica Typhimurium in cattle manure and manure slurry.

As in water and soil, Giardia survives less well than Cryptosporidium in manure. Giardia cysts in cattle feces were noninfective within 1 wk following freezing at -4°C and were infective for only 1 wk at 4 and 25°C (Olson et al., 1999). On the other hand, Cryptosporidium oocysts remained infective for >12 wk at -4°C, 8 wk at 4°C, and 4 wk at 25°C.

	CONCLUSIONS

TOP NOTES ABSTRACT INTRODUCTION MANURE HANDLING AND FOODBORNE... EFFECT OF INCREASED HOG... ENVIRONMENTAL SURVIVAL OF THE... CONCLUSIONS REFERENCES

 
Of those pathogens considered, E. coli O157:H7 was the most persistent organism in cattle manure regardless of the temperature and manure form (solid or slurry). On the contrary, Campylobacter and Giardia were the weakest survivors in manure. Readers can refer to Wang and Doyle (1998) and Kudva et al. (1998) for details on environmental survival of E. coli O157:H7. It is clear that storing manure as a slurry, solid, or compost before it is distributed on fields results in a significant reduction in pathogen concentration. As most pathogens survive freezing or low temperatures for significant periods of time, untreated manure should not be distributed on fields where there is a potential for runoff. The lack of scientific information on the survival of human pathogens in swine manure is an impediment in developing directions for changes to improve its handling. There is a pressing need to close information gaps on this subject. We hypothesize that it should be possible to eliminate the major bacterial and protozoan pathogens from bulk liquid manure holding systems by storage at 25°C for 3 mo. This recommendation is primarily based on cattle manure data and may change in other animal manure systems. While this approach may be inconvenient in some climates it should, nonetheless, serve as a guide for future work to evaluate additional factors (e.g., pH) that could be used to optimize the lethal effects of the time–temperature relationship on pathogens in stored manures. We contend that elimination of pathogens from manures used as fertilizer is a critical control point for managing the pathogen problem on crops used as feed and food and in managing the microbial safety of the water supply.

	NOTES

TOP NOTES ABSTRACT INTRODUCTION MANURE HANDLING AND FOODBORNE... EFFECT OF INCREASED HOG... ENVIRONMENTAL SURVIVAL OF THE... CONCLUSIONS REFERENCES

 
Sponsoring organizations: Manitoba Livestock Manure Management Initiative and Manitoba Rural Adaptation Council.

	REFERENCES

TOP NOTES ABSTRACT INTRODUCTION MANURE HANDLING AND FOODBORNE... EFFECT OF INCREASED HOG... ENVIRONMENTAL SURVIVAL OF THE... CONCLUSIONS REFERENCES

 

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