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Factors Associated with the Likelihood of Giardia spp. and Cryptosporidium spp. in Soil from Dairy Farms¹

R. S. Barwick^*, H. O. Mohammed^*, M. E. White^* and R. B. Bryant

^* Department of Population Medicine and Diagnostic Sciences, College of Veterinary Medicine, Cornell University, Ithaca, NY 14853, USA
Department of Soil, Crops, and Atmospheric Sciences, Cornell University, Ithaca, NY 14853, USA

Corresponding author:
H. O. Mohammed; e-mail:
hom1{at}cornell.edu.

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
A study was conducted to identify factors associated with the likelihood of detectingGiardia spp. and Cryptosporidium spp. in the soil of dairy farms in a watershed area. A total of 37 farms were visited, and 782 soil samples were collected from targeted areas on these farms. The samples were analyzed for the presence of Cryptosporidium spp. oocysts, Giardia spp. cysts, percent moisture content, and pH. Logistic regression analysis was used to identify risk factors associated with the likelihood of the presence of these organisms. The use of the land at the sampling site was associated with the likelihood of environmental contamination with Cryptosporidium spp. Barn cleaner equipment area and agricultural fields were associated with increased likelihood of environmental contamination with Cryptosporidium spp. The risk of environmental contamination decreased with the pH of the soil and with the score of the potential likelihood of Cryptosporidium spp. The size of the sampling site, as determined by the sampling design, in square feet, was associated nonlinearly with the risk of detecting Cryptosporidium spp. The likelihood of the Giardia cyst in the soil increased with the prevalence of Giardia spp. in animals (i.e., 18 to 39%). As the size of the farm increased, there was decreased risk of Giardia spp. in the soil, and sampling sites which were covered with brush or bare soil showed a decrease in likelihood of detecting Giardia spp. when compared to land which had managed grass. The number of cattle on the farm less than 6 mo of age was negatively associated with the risk of detecting Giardia spp. in the soil, and the percent moisture content was positively associated with the risk of detecting Giardia spp. Our study showed that these two protozoan exist in dairy farm soil at different rates, and this risk could be modified by manipulating the pH of the soil.

Key Words: risk • Cryptosporidium spp. • Giardia spp. • soil

Abbreviation key: OR= odd ratio

	INTRODUCTION

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Cryptosporidium spp. and Giardia lamblia are the two parasites responsible for causing the gastrointestinal disorders of cryptosporidiosis and giardiasis, respectively (Fayer, 1997). Both diseases are characterized by severe gastroenteritis and diarrhea, and symptoms may include diarrhea, abdominal pain, and even fever and vomiting (Fayer, 1997). The organisms can be transmitted through water and have been found to be prevalent in unfinished water sources (Madore et al., 1987; LeChavallier et al., 1991; Rose et al., 1991; Roach et al., 1993). Both organisms can survive modern drinking water treatments and have been implicated in several drinking water outbreaks throughout the world, including North America and the United Kingdom (Hayes et al., 1989; Smith et al., 1989; Joseph et al., 1991; Richardson et al., 1991; Rose et al., 1991; Leland et al., 1993; MacKenzie et al., 1995; Goldstein et al., 1996; Solo-Gabriele and Neumeister, 1996).

Cryptosporidiosis is transmitted by the ingestion of an infective oocyst which is shed through the feces of other infected hosts (Fayer, 1997). Cryptosporidium parvum and Cryptosporidium muris are the species most commonly associated with infection in humans and other mammals (Fayer, 1997). Cryptosporidium spp. has been found to be prevalent in mammals such as sheep, horses, goats, pigs, dogs, cats, and cattle (Anderson, 1991; Moore and Zeman, 1991; Mtambo et al., 1991; Xiao et al., 1993; Garber et al., 1994; Xiao and Herd, 1994; Atwill et al., 1997; Johnson et al., 1997; Muriuki et al., 1997; Olson et al., 1997; Wade et al., 2000). Through excretion and the process of manure spreading on farmland, these populations contaminate the environment. By contaminating the environment, dairy farms serve as a potential source of exposure of the human population to Cryptosporidium spp (Smith and Rose, 1998).

Like Cryptosporidium, Giardia is spread through the fecal-oral route, with the ingestion of Giardia cysts that can infect the small intestine of mammals. The organism reproduces in the host, and infective cysts are shed into the environment through the feces (Buret et al., 1990). Giardia has been found to be prevalent in bovine populations (Buret et al., 1990; Xiao and Herd, 1994; Olson et al., 1997) and, like Cryptosporidium spp., it is these populations that may serve as a source of contamination to water supplies as Giardia cysts travel through the environment.

Most of the research on these two organisms in the environment has focused on their presence in water sources (Madore et al., 1987; LeChavallier et al., 1991; Roach et al., 1993). However, the route of transmission of the Cryptosporidium oocyst or the Giardia cyst from the animal source to the water supply system through the environment must be determined in order to implement control strategies and ultimately prevent contamination of public water supplies. It has already been demonstrated experimentally that Cryptosporidium oocysts are able to move through various soil types (Mawdsley et al., 1996a) and resist environmental pressures such as temperature and pH, indicating its potential to contaminate and survive in the environment (Fayer and Leek, 1984; Robertson et al., 1992; Brown et al., 1996; Fayer and Nerad, 1996). Due to the ubiquitous nature of these organisms, an important step in the risk assessment framework for the protection of water quality is determining whether these two parasites are present in the soil surrounding water sources and determining and quantifying risk factors associated with their presence.

This study was designed to determine and quantify risk factors associated with the likelihood of detecting Cryptosporidium spp. oocysts or Giardia spp. cysts in the soil of dairy farms in the Catskill region of southeastern New York State.

	MATERIALS AND METHODS

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Study Population
The target population of this study was all dairy farms in southeastern New York State. The farms enrolled in this study had agreed to participate in an agricultural development program, whose goal was to maintain the quality of the water and sustain the economic viability of agriculture in the watershed in that area. At the time of the study, 40 farms agreed to participate in the program, 37 of which we visited.

Determination of Sampling Site and Soil Sample Collection
A detailed description of sampling site selection and sample collection was provided elsewhere (Barwick and Mohammed, 1997). Briefly, a multidimensional scale was used to identify sampling sites. This scale consisted of elements that are known or perceived by experts to be associated with the likelihood of the presence of Cryptosporidium spp. or Giardia spp. in these sites. Criteria included in this scale included information about potential contamination sources, such as young stock, proximity to those perceived contamination sources, animal density, and geography of the area. This scale allowed us to apply a numerical level of contamination risk to a geographical area. Only one observer scored each risk area on a farm to reduce interobserver variability. Scores were standardized to control for intraobserver variability from farm to farm.

Once this scale was applied, we were able to characterize these areas into high, moderate, and low likelihood zones. Zones were categorized according to their score as follows: 74 high likelihood zone >45; 45 moderate likelihood zone >15; and low likelihood zone 15. The highest likelihood zone was identified as the sampling area for that farm.

Dairy farms enrolled in the study were visited to collect soil samples and to administer a questionnaire to farm owners. Soil samples were collected by inserting a 3-in diameter stainless steel ring to a depth of 2 in at selected sampling sites. The ring was pushed into the ground and the sample was placed in a sealable plastic bag and properly labeled. Samples were transported back to Cornell University for parasite, pH, and percent moisture content analysis. At the time of the farm visit, the farm owner was interviewed, and data on the hypothesized risk factors were collected using a questionnaire. These factors included information on the sampling site, farm demographics, and management practices and are listed in Table 1.

Statistical Analysis
From the data collected during the farm visit, risk factors associated with the likelihood of detection of Cryptosporidium spp. oocysts and Giardia spp. cysts in the farmlands of southeastern New York State were identified using ordinary logistic regression (Dixon, 1992). Our outcome variable was dichotomous, presence or absence of the organism in the sample. Initially, the bivariate association between each factor and the likelihood of detecting the organism was evaluated in a univariate logistic regression model. The logistic regression model used is as follows:

whereP(D) is the probability of presence of a cyst or oocyst in the sample; is the log odds of cyst or oocyst in the sample with standard set of factors, and ßiis the effect of the respective factor Xi on the likelihood of detecting the cyst or oocyst in the sample. The significant level of the initial screening was at aP value 0.10. The magnitude of the effect of a factor was quantified by the odds ratio (OR). The OR is the odds of recovery of a particular protozoa under the presence of the factor in comparison to the odds of recovery in absence of the factor.

Factors that were significantly associated with the likelihood of the organism in the initial screening were further evaluated jointly in a multivariate analysis. A forward stepping with backwards elimination logistic regression analysis approach was used to identify those variables associated with the risk of detection of C. parvum in the soil (P 0.10).

Because the sampling units were clustered by farm, we hypothesized that the clustering might lead to a correlation in the likelihood of these organisms. This hypothesized correlation between samples is due to observed and unobserved farm factors. Conditioning on an observed set of these factors by including them in the logistic regression analysis will sometimes achieve approximate conditional independence. We assumed that the unobserved factors are randomly distributed among farms in the study population, and the significance of this assumption was evaluated using the mixed effect logistic regression analysis (Atwill et al., 1995). The mixed effect model was specified as follows:

whereP(Dij/,ß_k,) is the probability of the presence of a cyst or an oocyst in individual samplej located within random effect leveli (e.g., farm); was the natural logarithm of the odds of testing positive under standard circumstances; and ß_kwas the change in the natural logarithm of the odds for developing the disease for a unit change in the risk factor,X_k; and µ_i ^{was the farm random effect.}

	RESULTS

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A total of 782 soil samples were collected from 37 farms throughout southeastern New York State. We examined risk factors including information on the farm, the management practices of the farm, and particular specifics of the sampling site (Table 1).

Cryptosporidium spp.
Risk factors were identified to be associated (P 0.10) in a multivariate analysis with the risk of detectingCryptosporidium spp. in the soil. Categorical factors, their adjusted OR, and corresponding 90% confidence intervals are listed in Table 2.

There was a significant association between the size of the sampling site and the risk of detection of Cryptosporidium spp. oocysts. The risk decreased as the size of the zone increased, reached the minimum value at 190 sq ft, and then increased (Table 2). There was no significant clustering in the likelihood of detectingCryptosporidium spp. by farm, as determined by the mixed effect model.

Giardia spp.
Factors significantly associated with the likelihood of detecting aGiardia spp. cyst in the univariate model are listed in Table 3.The likelihood of detectingGiardia cysts in the soil samples increased with the prevalence of the organism in the herd. There was also a 5.24 times greater likelihood of detectingGiardia in the soil when cattle had access to the sampling site compared with sites where cattle did not have access. Vegetation at the sampling site was significantly associated with the risk of detectingGiardia in the soil. Areas that were brush or bare soil were less likely to test positive forGiardia than land that had managed grass. Managed grass sites were managed or less weedy that areas which were categorized as weeds and grass. These sites were not managed or had spontaneous growth.

The random effect of the farm was not significantly associated with the likelihood of detecting a Giardiacyst.

	DISCUSSION

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Giardiaspp. andCryptosporidiumspp. have been implicated in several drinking water outbreaks of giardiasis and cryptosporidiosis, respectively. As waterborne pathogens, one potential route of transmission from the animal to the water system is through the soil (Smith and Rose, 1998). Because bothGiardiaspp. andCryptosporidiumspp. have a wide range of hosts, their eradication is unlikely, and efforts to prevent water contamination should focus on the control of these pathogens. To date,Cryptosporidiumis able to survive most modern drinking water treatments, and until methods are developed to ensureCryptosporidium-free water, attention should be focused on preventing the oocyst from entering the water supply system (Smith and Rose, 1998). Soil could be an important vehicle through which theCryptosporidiumoocyst andGiardiacyst can travel into water sources (Smith and Rose, 1998). To design effective prevention strategies, it is important to develop a base knowledge about the factors that play a role in the transmission and contamination of the water supply system. This study represents a step towards that goal. To our knowledge, there is no published study investigating risk factors associated with the presence ofGiardiaorCryptosporidiumin the soil of dairy farms. Other studies have identifiedCryptosporidium spp. andGiardiaspp. in water sources but not in soil (Madore et al., 1987; LeChavallier et al., 1991; Roach et al., 1993), and several studies have looked at risk factors related to these organisms but not in soil.

Our sampling design targeted those areas that were identified by the multidimensional scale to have the highest risk of contaminating the environment on a particular farm (Barwick and Mohammed, 1997). This sampling scheme allowed us to assess high-risk areas quantitatively and systematically and provided a feasible design. Furthermore, it allowed us to weigh the sampling towards a high-risk area and utilize our resources efficiently. It was designed to make inferences about the presence of the organisms and factors associated with them. This scale also allowed us to avoid the problem of multicolinearity. Multicolinearity may develop when correlated variables play a role on the risk of a particular outcome, in our case, detection of an oocyst or cyst. This scale allowed us to examine multiple variables and avoid this problem.

Samples were evaluated using an adaptation of the flotation technique, and we determined a sample to be positive for Cryptosporidiumspp. orGiardiaspp. if at least one oocyst or cyst was detected (Atwill et al., 1997; Barwick et al, 2000). Although this procedure does not conclude organism viability, oocysts and cysts were evaluated on size, shape, and internal structure, which have been used to indicate viability (Le Chavallier et al., 1991b). Additionally, this method does not identify species ofCryptosporidiumor the source of the organism. The oocysts we observed were found in areas believed to be contaminated by cattle, but it is possible that other animals may have been responsible for shedding the oocysts, such as wildlife or domestic animals with access to the area.

It was previously reported that the prevalences of Giardiaspp. andCryptosporidiumspp. in the soil of these dairy farms were found to be 4 and 17%, respectively (Barwick and Mohammed, 1997). In these herds, the prevalence ofGiardiawas as high as 39% (Wade et al., 2000); thus, it was unexpected that the prevalence ofGiardiain the soil would be low. This might be explained by the fact thatGiardiais not as resistant to environmental pressures asCryptosporidiumand may not be able to survive for long periods (Rings and Rings, 1996).

In the multivariate analysis, three categorical factors were found to be significantly associated with the likelihood of detecting Cryptosporidiumspp. in the soil. The use of the land was significantly associated with the risk of detectingCryptosporidiumspp. oocysts in the soil. The finding that area around barn cleaners and agricultural fields had an increased risk for detecting oocyst compared with land that was not used was consistent with expectations. One would expect that these areas may have large concentrations of manure, particularly when the agricultural field has been spread with fresh manure. We were not able to demonstrate significant association between the prevalence ofCryptosporidiumspp. in the animals on the farm and the likelihood of detecting the organism in the soil. One plausible explanation is that the animal sampling was from the animals directly, whereas the soil sampling is cumulative sampling.

The pH of the soil was significantly associated with the likelihood of detecting Cryptosporidiumspp. The risk of detecting the oocyst decreased with increasing levels of pH (Table 2). Samples in the neutral category (pH 6.5 to 7.5) were 0.53 times less likely to have aCryptosporidiumoocyst, and those in the basic category (pH 7.6 to 9.75) were 0.35 times less likely, compared with those samples in the acidic category (pH 3.7 to 6.4). This finding is not consistent with what is reported in the literature (Robertson et al., 1992; Brown et al., 1996). Interestingly, other studies have shownCryptosporidiumoocysts unable to survive low extremes of pH (Robertson et al., 1992; Brown et al., 1996).

The continuous variables for sampling site size were linearly and nonlinearly associated with the detection of Cryptosporidiumspp. in the soil. It appeared as though as the size of the sampling site increased, risk of detection decreased and then began to increase when the sampling site was above 190 sq ft. It is possible that this association is due to the use of the land site or may serve as a proxy for an unmeasured variable relating to the size of the sampling site.

The random effect variable was not significant in this final model. This can be interpreted that the three factors included in this final model account for all the variability in the presence of the oocyst in the soil, or we did not have much variability among our samples.

Several factors were significantly associated with the likelihood of detecting a Giardiacyst in the soil in the univariate analysis. However, none of the factors was significant when we used the multivariate analysis. An obvious explanation is that the prevalence ofGiardiain our samples was relatively low, and as a consequence, we were not able to evaluate two factors jointly. The strongest association existed between detection of a cyst and the prevalence ofGiardiain the herd. The prevalence ofGiardiainfection in the herd was obtained through a prevalence study (Wade et al., 2000), and we found that farms that had a prevalence rate of 18 to 39% were seven times more likely to have soil that tested positive. This is not surprising and supports the conclusion that the cattle were the source of the cysts identified. Whether or not the cattle had access to the area was also strongly associated with the detection of a cyst. Areas that cattle could access were 5.24 times more likely to containGiardiacysts than those areas to which cattle did not have access. Again, this finding is not surprising in that althoughGiardiacysts are commonly shed by young stock, it has been found in animals up to and beyond 6 mo of age (Xaio et al., 1993; Xaio and Herd, 1994; Olson et al., 1997). One significant variable that was surprising was the number of cattle <6 months of age. This was negatively associated with the risk of detecting a Giardia cyst in the soil. That is, as the number of cattle on the farm <6 mo of age increased, the likelihood of detecting aGiardiacyst decreased. This was unexpected, as it is generally the younger animals that tend to be more likely to shedGiardia(Xaio and Herd, 1994; Olson et al., 1997). Another factor significantly associated with detecting aGiardiacyst was the vegetation of the sampling site. Land covered with brush or bare soil was 0.273 less likely to have cysts than land with managed grass. It is possible this is because areas without vegetation allow for easier runoff, decreasing the likelihoodGiardiawould be found there. Also, land with vegetation decreases the rate of evaporation, and soil will stay wet longer, and it has been suggested thatGiardiaconcentrations are higher in wetter soil (Hu et al., 1996). More evidence that soil water content plays a role in detectingGiardiawas the significance of percent moisture content of the soil. We found that as the percent moisture content increased, the likelihood of detecting a cyst increased also. This agrees with findings by Hu et. al. (1996), who investigated the role ofGiardiain sludge mixed with soil. They found thatGiardiaconcentrations decreased in sludge mixed with soil, and they felt this was primarily due to low-moisture content. Another plausible explanation for the absence ofGiardiafrom soil collected from bare or brush areas could be attributed to low grazing intensity and hence, less likelihood of fecal excretion.

As part of our analysis, we included the random effect of the farm into our model to examine for any presence of intragroup correlation among the farms. For both CryptosporidiumandGiardia, it was interesting that the effect of the farm was not significant. For the model based on the risk of detectingCryptosporidiumspp., this may be because there was a fairly high farm prevalence, with 92% of the farms testing positive forCryptosporidiumspp. (Barwick and Mohammed, 1997).

In conclusion, we found that land use and pH were associated with the risk of detecting Cryptosporidium spp. in the soil. Herd prevalence, vegetation, moisture content, and cattle access were significantly associated with the likelihood of detecting Giardia spp. in the soil. Future research should be conducted to fully understand the roles these factors play on the existence of these parasites in the soil and help to implement practices which could help to reduce the transmission of these two organisms.

	FOOTNOTES

 
¹ Supported partially by grants from the USDA Formula Funds, New York State Department of Environmental Protection, The Watershed Agricultural Council, and the Water Resources Institute, Cornell University.

Received for publication August 27, 2002. Accepted for publication November 3, 2002.

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